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1 VOLUME XXVIII, NUMBER 1-4, SPECIAL ISSUE (PUBLISHED APRIL 2014) Neonicotinoids, Bees, Birds and Beneficial Insects

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Page 1: Neonicotinoids, Bees, Birds and Beneficial Insects · Bumble bees and other native bees are also dying (Whitehorn et al. 2012). Part of the problem is expo-sure to systemic insecticides

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VOLUME XXVIII, NUMBER 1-4, SPECIAL ISSUE (PUBLISHED APRIL 2014)

Neonicotinoids, Bees, Birds and Beneficial Insects

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© 2014 Bio-Integral Resource Center. All rights reserved. ISSN 8756-7881

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By William Quarles

About one-third of managedhoney bee colonies in theU.S. are dying each year (van

Engelsdorp et al. 2012; NAS 2007).Bumble bees and other native beesare also dying (Whitehorn et al.2012). Part of the problem is expo-sure to systemic insecticides calledneonicotinoids. Insecticides are nor-mally applied in ways to mitigatetheir impact on bees, but mitigationstrategies are not possible with sys-temics because they are alwayspresent in the plant. Each year,over 146 million acres (59 millionha) of crops in the U.S. are treatedwith neonicotinoids. This representsabout 45% of the total cropland,and acreage is increasing each year(Stokstad 2012; Spivak et al. 2011;Quarles 2011; Quarles 2008).

Found EverywhereNeonics are used in field crops,

orchards, parks, landscapes, back-yard gardens, on ornamentals,lawns, pets, and in structural pestcontrol. Neonics are applied asfoliar sprays, soil drenches, gran-ules, tree injections, and as seedtreatments. Some of them areextremely persistent, providing abig window of possible exposure.They can remain active in soil formore than a year after application,or for several years inside trees.Neonics are found in pollen andnectar of treated plants, in leaf lit-ter, soil and water. The problem isthat they are found everywhere,even in bee friendly plants pro-duced by horticultural nurseries(Goulson 2013; Hopwood et al.2013).

Beneficial InsectsWidespread exposure to neoni-

cotinoids is killing beneficial insectssuch as ladybugs and parasiticwasps. Beneficial insects are killedby acute exposure to neonic spraysand by chronic exposure to poi-soned prey and the poisonouspollen and nectar of systemicallytreated plants (Hopwood et al.

2013). The economic effect is sub-stantial. Biocontrol is worth morethan $4 billion a year to agricul-ture, and honey bees plus nativebees provide up to $19 billon of pol-lination services. The value provid-ed by these insects far exceeds the$2.6 billion of neonicotinoid sales(Losey and Vaughn 2006; Jeschkeet al. 2011).

Birds Also KilledNeonicotinoids are also killing

birds. A major route of exposure isthrough seed treatments. Somebirds can be killed by eating justone poisoned seed (Mineau andPalmer 2013). Most of U.S. corn,soybeans, cotton, cereals, sugarbeets, sunflowers, oilseed rape andother crops are grown with neoni-cotinoid seeds (Elbert et al. 2008).Though seed treatments preventpesticide drift and the environmen-tal problems of sprays, the vastacreage of exposure is becoming aproblem (Goulson 2013).

Pollute WaterAbout 2-20% of a seed treatment

is absorbed by the plant. The rest iseither blown into the air by seeddrills, or remains in soil. The toxicairborne dust from seed drills cankill flying bees and ultimately pol-lutes non-target plants and soil.Seed treatments and soil drenchesare finally washed away into groundand surface water (Goulson 2013;Krupke et al. 2012).Neonicotinoids allow growers to

ignore good farming methods andIPM approaches in favor of systemicprotection. With the IPM method,pesticides are applied only afterpests appear and economic thresh-olds are reached. But seed treat-ments are applied before pests areseen, and may not be needed. Thisapproach can lead to unnecessaryexpense and no improvement inyield in years of low pest pressure(Gray 2011; Seagraves andLundgren 2012). This article reviews the some of

the environmental problems causedby neonicotinoids, and the nextarticle suggests IPM alternatives.

What are Neonicotinoids?Neonicotinoid pesticides are

analogs of the neurotoxin nicotine,and some of their actions are simi-lar. They are neurotoxins that inter-fere with the acetylcholine nervoussystem that is essential for life.They disturb nerve function bybinding to nicotinic receptors. Theybind more strongly to nicotinicreceptors in insects and are thusmore toxic to insects than mam-mals. This selectivity caused regula-tors to view them favorably(Tomizawa and Casida 2003). Neonicotinoids also show inverte-

brate species selectivity, which canbe either a blessing or a curse.They are especially effective forsucking pests such as aphids,whiteflies, planthoppers, and thrips.They also provide protection fromborers, caterpillars, beetles, and thecorn rootworm (Elbert et al. 2008).But honey bees and parasitic waspsare extremely sensitive, and neoni-cotinoids will not kill pest mites orticks. So careless treatments withneonics can kill bees and lead topest mite explosions (Jeschke et al.2011; Szczepaniec et al. 2013). In the U.S. there are now six

commercially available neonicoti-noids: imidacloprid, clothianidin,thiamethoxam, acetamiprid, dinote-furan, and thiacloprid. They differsomewhat in water solubility, sys-temic action, selectivity and persist-

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Honey bees, Apis mellifera, canbe killed by neonicotinoids.

Photo co

urtesy

of K

athy Keatley

Garvey

Neonicotinoids, Bees, Birds and Beneficial Insects

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ence. As we see in Table 1, imida-cloprid, clothianidin and thi-amethoxam are more acutely toxicto bees and are the most persistent. The selectivity, systemic action,

and persistence that made thempopular are now causing problems.They are killing birds, bees, andbeneficials, and due to overuse andpersistent exposure, some of theinsect pests are becoming resistant(Jeschke et al. 2011; Mineau andPalmer 2013).

Problems with BeesBees can be killed by neonicoti-

noid foliage sprays, by poisonousdust from seed planting machines,by treated irrigation water, and byexposure to poisonous pollen andnectar from systemically treatedplants (Quarles 2011; Goulson2013; Blacquiere et al. 2012;Hopwood et al. 2012; Krupke et al.2012). Environmental problems with

pesticides can be dramatic. In Juneof 2013, about 50,000 bumble beeswere killed when linden trees inOregon were sprayed with the neon-icotinoid pesticide dinotefuran(Black and Vaughn 2013). In May of2008, about 50% of honey bees inthe German state of Baden-Wurttemberg were killed by theneonicotinoid pesticides clothiani-din and imidacloprid, which hadbeen applied to seeds. According tothe manufacturer, farmers appliedthese pesticides without using theadhesives recommended to keep thepesticides localized to seeds (EPA2008; Hopwood et al. 2012).

Bees Extremely SensitiveBees are extremely sensitive to

neonics and can be exposed forlong periods to plants full of sys-temic toxins. As we see in Table 1,just 3-4 billionths of a gram (3-4ng) of imidacloprid or clothianidinis enough to kill a honey bee.Neonics can impact bee populationsthrough direct mortality andthrough sublethal effects on behav-ior, such as impaired memory,learning and foraging. Impaired for-aging can lead to poor nutrition,and pesticides may directly impactbee immune systems, making themmore susceptible to disease. In

addition, sublethal pesticides inter-fere with brood development andshorten lifespans of adults (Henryet al. 2012; Pettis et al. 2012; Wu etal. 2011; Desneux et al. 2007).

Lethal Doses in the FieldsFlying bees are killed by aerially

dispersed seed coatings and talcfrom seed planting machines(Krupke et al. 2012; Marzaro et al.2011; Tapparo et al. 2012; Girolamiet al. 2012). Poisonous dust fromplanting machines can also con-taminate flowers, pollen, and leafsurfaces of non-target plants, soil,and water. Pesticide persistenceguarantees longterm exposure(Goulson et al 2013). Bees may be killed by guttation

water from treated plants. Cornexcretes droplets of water along leafmargins called guttation drops. Forabout three weeks after emergence,droplets from seed-treated corncontain concentrations of neonicoti-noids lethal to bees (Girolami et al.2009). Levels in guttation fluid canbe 254 times the bee LD50 for imi-dacloprid, 280 times the LD50 forclothianidin and 48 times the LD50for thiamethoxam (Thompson2010). Lethal guttation drops arealso found in melon crops withneonicotinoid soil treatments(Hoffman and Castle 2012).

Exposure in Bee HivesBee exposure to pesticides is

widespread. Mullin et al. (2010)checked a large number of commer-cial bee hives for pesticides. Hivesfrom 23 states including Florida,California, Pennsylvania and migra-tory bees from East Coast colonieswere analyzed. Wax, pollen, andbees were highly contaminated with

pesticides. There were 121 differentpesticides and metabolites in 887wax, bee, and pollen samples, aver-aging about 6 pesticides per sam-ple. Mullin et al. (2010) found bee

pollen in hives contained imidaclo-prid at a median concentration of20 ppb (ppb is parts-per-billion)and a maximum concentration of206 ppb. These levels are known toimpact the health of bees. A total of43 pollen samples (12%) out of 350contained neonicotinoids or theirmetabolites. Mullin et al. were ana-lyzing hives foraging on specialtycrops such as citrus, apples andothers that do not use seed treat-ments. Where bees forage on cropssuch as corn, canola, or sunflowersthat use neonicotinoid seed treat-ments, 50% of pollen samples car-ried by honey bees can be contami-nated with these pesticides (Krupkeet al. 2012; Lu et al. 2012;Blacquiere et al. 2012).Nurse bees feed contaminated

pollen to larvae. Sublethal concen-trations of neonicotinoids and otherpesticides in brood comb can delaydevelopment of adult bees. Delayed

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Commercial hives are heavilycontaminated with pesticides.

Photo co

urtesy

of K

athy Keatley

Garvey

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development can make the beesmore susceptible to mites.Pesticides in the brood comb alsoshorten life span of adult bees (Wuet al. 2011).

Sublethal and Lethal Effects

Sublethal effects such as reducedfeeding have been found in adultbees upon ingestion of 6 ppb or lessof imidacloprid. Reduced feedingcould lead to poor nutrition.Longterm feeding of 4-40 ppbimpairs olfactory learning, which isassociated with finding food(Decourtye et al. 2001; 2004). Toxicity is cumulative, and one

experiment showed 50% mortalitywhen adult bees were fed 0.1 to 10ppb imidacloprid for 10 days(Suchail et al. 2001ab). Otherexperiments have shown that mor-tality starts at feeding levelsbetween 24-48 ppb (Decourtye et al.2004). Field tests have shown thathives can be killed by feeding at 20ppb (Lu et al. 2012).

Cause DiseaseSublethal exposure to neonicoti-

noids can depress immune functionin bees and other wildlife, leading todiseases. Imidacloprid and clothian-idin trigger production of proteinsthat suppress immune function,making bees more susceptible todeformed wing virus. Bees exposedto imidacloprid are more suscepti-ble to infections with the Nosemapathogen. Beetle grubs treated withimidacloprid are more easily killedby pathogenic nematodes (Pettis etal. 2012; Kopenhofer et al. 2002; diPrisco et al. 2013). Other examplescan be found in Mason et al.(2013).

Synergism and LarvalExposure

Careless use of fungicides isadding to problems with neonics.Fungicides such as chlorthalonilare often sprayed on floweringplants. Adult bees are not killed,but foragers take contaminatedpollen and nectar to the hive to feedlarvae. Bee larvae are more sensi-tive than adult bees to pesticides.Zhu et al. (2014) found that realis-

tic hive exposures of chlorthalonilcould make some insecticides seventimes more toxic to bee larvae.A number of other studies have

noted the synergistic interaction offungicides with neonics (Schmucket al. 2003; Isawa et al. 2004), andother insecticides (Johansen 1977;Atkins 1992; Pilling and Jepson1993). Sublethal exposures of neon-ics can be amplified by synergisticinteractions with fungicides andother pesticides, poisoning larvaeand eventually killing bee colonies(Zhu et al. 2014).

Exposure to Nectar and Pollen

Bees can be exposed to contami-nated nectar and pollen of neonictreated plants. Chronic doses canaccumulate because bee metabo-lism and elimination of neonicoti-noids such as imidacloprid (IMD) is

slow. One of the IMD metabolites istwice as toxic as IMD (Chauzat etal. 2006). Metabolism is complexand thiamethoxam is actually con-verted by metabolism into clothiani-din (Hopwood et al. 2012; Krupke etal. 2012).Imidacloprid (IMD) is often

applied as a seed treatment.Average concentration in pollen ofseed-treated sunflowers, corn, andrape is usually 10 ppb or less, butindividual plants can have 18 ppbor more. Flowers can have higherconcentrations than pollen,amounts in nectar are usually lessthan 5 ppb (Laurent and Rathahao

2003; Fossen 2006; Bonmatin et al.2005). Average amounts from sever-al seed treatment studies are 6.1ppb in pollen and 1.9 ppb in nectar(Goulson 2013).Seed treatments of neonicotinoids

can cause sublethal effects (Boily etal. 2013). At the least, field realisticlevels in nectar from seed treat-ments can reduce expected per-formance in adult honey bees bybetween 6 and 20% (Cresswell2011). Sublethal concentrations inthe hive interfere with brood devel-opment (Wu et al. 2011).

Exposure Greater fromSoil Treatments

Relatively small amounts of neon-ics appear in pollen and nectarfrom seed treatments. But neoni-cotinoids are also used as foliarsprays, as soil drenches, and fortreating landscape ornamentals aswell as crop plants. Amounts usedon ornamentals lead to residues 12-16 times greater than found oncrop plants (Hopwood et al. 2012).Concentrations up to 66 ppb arefound in pollen, and up to 23 ppbin nectar (Goulson 2013). Soil treat-ments in eucalyptus led to concen-trations of 660 ppb in pollen (Paineet al. 2011). Foliar sprays duringflowering could have disastrousresults. Up to 147 ppb of neonicshave been found in pollen of flower-ing pumpkin, and concentration innectar was up to 11 ppb (Goulson2013).

They Never ReturnYang et al. (2008) found that con-

centrations of imidacloprid of 40-50ppb in sugar water were enough tocause impaired foraging of honeybees in the field. Nectar concentra-tions from seed treatments arelower than this, but even if nectarconcentrations are low, fairly largechronic doses can be delivered. Abee ingests 20-30 µl of nectar eachtime, and the half life of IMD isabout 4.5 hrs, making chronicaccumulation possible. Since beesingest average nectar loads of 40mg, and eat about 11.5 mg/hr,about 2 ng of imidacloprid can beaccumulated from feeding for 3 hrsat 50 ppb. Imidacloprid is metabo-lized by bees into toxic metabolites

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This hive is dead due to ColonyCollapse Disorder.

Photo co

urtesy

of K

athy Kea

tley Garvey

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that can also accumulate (Suchailet al. 2003; 2004; Cresswell 2011;Faucon et al. 2005; Quarles 2011).The relatively small amount in

pollen and nectar can disorientbees and lead to field losses. Henryet al. (2012) treated honey beeswith sublethal 1.3 ng doses of thi-amethoxam. About 10% of treatedbees released in familiar surround-ings failed to make it back to thehive. About 32% of treated beesreleased in unfamiliar surroundingsfailed to return. Field impact stud-ies often put hives immediatelyadjacent to treated fields to assesseffects. This study shows that thismethod would tend to underesti-mate pesticide induced foragingimpairment (Henry et al. 2012;Quarles 2011).Schneider et al. (2012) found that

26% of foragers did not return afteroral doses of 1 ng (one-billionth of agram) of clothianidin, and 79% didnot return after 2 ng. Matsumoto(2013) found that successful hom-ing flights of honey bees werereduced at doses of 1/10 the LD50of clothianidin and dinotefuran.

Bumble Bees also AffectedSublethal doses of IMD have been

shown to affect bumble bee forag-ing. After 9 days of foraging in sun-flowers treated with IMD, about10% more bumble bees were lost inthe field compared to bumble beeforagers in untreated fields (Taséi et

al. 2001). Larson et al. (2013)sprayed clothianidin on lawns withflowering clover. Concentration ofthe pesticide in clover nectar wasabout 170 ppb. There wasdecreased bumblebee foraging,

increased mortality, and no newqueens were produced.Whitehorn et al. (2012) fed 25

bumble bee colonies in the labora-tory for 14 days on pollen contain-ing 6 ppb imidacloprid and sugarwater containing 0.7 ppb. Colonieswere then left to forage in the fieldfor six weeks. After six weeks, treat-ed colonies weighed 8-12% lessthan untreated controls. The weightdrop was likely due to pesticideinduced impairment of food gather-ing efficiency. Treated colonies alsohad on average about 85% fewerqueens.

Delayed MortalityMost of the bee toxicity experi-

ments are done either on individualbees or on hives monitored for alimited amount of time. Lu et al.(2012) chronically dosed summerbees with imidacloprid, thenstopped. Mortality was delayed forseveral months. Bees were fed high fructose corn

syrup containing 20, 40, 200, and400 ppb imidacloprid. About 23weeks (nearly 6 months) after thelast dose, 15 of 16 of the treatedhives were dead. Dead hives had nobees, but still had food. Summerbees were fed imidacloprid, and thewinter bees died. This kind of delayed mortality

mimics some of the manifestationsof Colony Collapse Disorder. Thelowest feeding dose was 20 ppb.Earlier experiments had shown noeffect on overwintering bees whensummer bees were fed 5 ppb of imi-dacloprid in sugar syrup. Therewere four untreated control hives,and three of four survived (Fauconet al. 2005; Lu et al. 2012).

Bans in EuropeThe adverse effects of neonicoti-

noids on bees have led to severalbans in Europe. In 1994, aboutthree years after imidacloprid wasintroduced, French beekeepersnoticed large losses of bees. Thesebees had been foraging in sunflowercrops whose seeds had been treatedwith imidacloprid. Imidacloprid onsunflowers was banned in France in1999, followed by a ban of use oncorn in 2004. Germany and Italybanned neonics on corn in 2008.The possible connection between

bee destruction and neonics led toa two-year ban of some neonics inthe European Union in 2013(Hopwood et al. 2012; EPA 2013).

Effects on BeneficialsThat broadspectrum pesticides

can have effects on beneficialinsects such as ladybugs is not newor surprising. However, because ofthe multiple routes of application,beneficials can be exposed to neoni-cotinoids in a number of differentways. Because of persistence, neon-ics provide both acute and chronicexposures. Also, neonics are moretoxic than older pesticides to somebeneficials (Cloyd et al. 2009;Hopwood et al. 2013).Beneficials are killed by exposure

to foliage sprays of neonicotinoidsand exposure to residues. They arekilled through secondary poisoningwhen they ingest aphids and otherpests that have been poisoned withneonicotinoids. Soil applications ofneonicotinoids lead to relativelyhigh systemic concentrations inplant nectar, leading to death ofparasitoids (Krischik et al. 2007).Soil applications also kill grounddwelling beneficials such as groundbeetles and earthworms. Even seedtreatments can have an impact onbeneficial populations (Seagravesand Lungren 2012).

Exposure to Sprays and Residues

Spray applications of the neonicsdinotefuran, acetamiprid, and cloth-

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Convergent lady beetle,Hippodamia convergens

Bumble bee, Bombus sp.

From Nixon 1954

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ianidin are highly toxic to the para-sitoid Leptomastix dactylopii andthe mealybug destroyer,Cryptolaemus montrouzieri. Thesebeneficials provide mealybug bio-control (Cloyd and Dickinson 2006). Predatory bugs such as nymphs

and adults of the soldier bug,Podisus maculiventris, are killed byimidacloprid sprays (De Cock et al.1996). Contact with label rates ofacetamiprid, thiamethoxam, andimidacloprid can kill all life stagesof the lady beetle, Harmoniaaxyridis (Youn et al. 2003). Thesebeneficial insects kill a wide rangeof insect pests.

Poisonous PreyCottony cushion scale poisoned

by systemic or foliar treatments ofcitrus with imidacloprid is toxic tothe predatory vedalia beetle, Rodoliacardinalis. Adult survival, progeny,and larval development are reduced(Grafton-Cardwell and Gu 2003). Imidacloprid soil treatments of

bean plants produce aphids, Aphisfabae, that are toxic to predatorylady beetles, Hippodamia undecim-notata. There is increased mortality,decreased longevity and egg pro-duction (Papachristos and Milonas2008).

Soil TreatmentsSoil treatments of neonicotinoids

can kill beneficials that dwell in thesoil. Imidacloprid is toxic to earth-worms at 2.3 to 3.48 ppm in drysoil (Wang et al. 2012), and sprays

of imidacloprid or clothianidin toturf at label rates can significantlyreduce earthworm populations(Larson et al. 2013; Kunkel et al.1999). Soil treatments can cause prob-

lems with predatory ground beetles.Neonicotinoid soil drenches aremore toxic than the organophos-phate chlorpyrifos to the beneficialsoil predator Atheta coriaria (Cloydet al. 2009). Beneficial ground bee-tle populations can be reduced by84% by imidacloprid granulesapplied to turf. After a year, popula-tions still had not recovered (Peck2009).

Killed By Systemics in Plants

Until recently, many professionalsbelieved neonicotinoids applied bysoil drenches were safe for benefi-cials. But because neonicotinoidsare systemic, root uptake leads toinsecticides in leaves, pollen, andnectar. Some beneficials are killedwhen they ingest poisoned pollen,nectar, and plant tissues to supple-ment their diet (Hopwood et al.2013).Various experiments have shown

there is 96% mortality of bumblebees foraging on flowers of treatedtomato, 38% mortality of ladybugsforaging on treated sunflowers, and86% mortality of adult lacewingsforaging on flowers of systemicallytreated buckwheat. Imidaclopridconcentration in the buckwheatflowers was 15 ppb (Rogers et al.2007).Another experiment showed that

buckwheat treated with imidaclo-prid soil drenches contained 16 ppbof imidacloprid in the flowers.About 88% of the parasitoids,Anagyrus pseudocci, that fed onnectar showed poisoning symptomsand 100% of them were dead withinseven days (Krischik et al. 2007).Adult Monarch butterflies,

Danaus plexippus, feed on plantnectar. Though research has notbeen published, it is likely thatmigratory butterflies may be affect-ed by systemic neonicotinoids(Goulson 2013).Eucalyptus trees, E. rudis, treated

with soil applications of imidaclo-prid at label rates had 660 ppb of

imidacloprid and its toxic metabo-lites in the nectar five months afterthe application. This amount is wellabove lethal concentrations forhoney bees. Parasitoids, such asAventianella longoi and Syngasterlepidus are killed by the nectar.Concentrations in the nectar were2-3 times the LC50 for the para-sitoids (Paine et al. 2011).Citrus leaves treated with sys-

temic applications of imidaclopridand thiamethoxam are toxic topredators and parasitoids. Contactwith treated leaves kills parasitoidssuch as Aphytis melinus andEncarsia formosa within four days,predators such as the minute piratebug, Orius insidiosus and the

bigeyed bug, Geocoris punctipes diewithin ten days (Prabhaker et al.2011).Systemic applications of imidaclo-

prid in citrus kills parasitoids suchas Aphytis melinus that are helpfulfor scale control (Grafton-Cardwellet al. 2008).

Seed TreatmentsThough soil treatments are more

deadly, seed treatments can havean effect on beneficial insects. Asdiscussed earlier, concentration ofimidacloprid in pollen from seedtreatments in crops such as cornand sunflowers, can range from 2to 20 ppb. Amounts in leaves andflowers can be higher. Some benefi-cials need to supplement their dietby feeding on plants, and this canbe deadly (Quarles 2011).

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Big-eyed bug, Geocoris punctipes

Pirate bug, Orius insidiosus

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Seagraves and Lundgren (2012)found that soybean seed treatmentsof neonicotinoids had little effect onpests such as soybean aphids, butsignificantly reduced numbers ofgeneralist predators such as nabidbugs and lacewings. Soybean yieldswere not improved, and thi-amethoxam reduced the beneficialpredator population by 25%.Seed treatments can kill ladybugs

that supplement their diets by feed-ing on the developing plants. About72% of Harmonia axyridis larvae ontreated corn plants developed neu-rotoxic symptoms, and most ofthem died. Plants grown from cloth-ianidin treated corn seeds killed80% of the exposed larvae; thi-amethoxam plants killed 53%(Moser and Obrycki 2009).There was 100% mortality in 17

of 18 species of beneficial carabidground beetles exposed to cornseedlings sprouted from neonicoti-noid seeds. Ground beetles such asHarpalus pensylvanicus are preda-tors of the corn rootworm andmany other destructive pests(Mullin et al. 2005).

Other EffectsSpider mites, Tetranychus urticae,

are not susceptible to neonicoti-

noids. Neonicotinoids may reducenatural inducible plant defensesagainst arthropods, leading to miteinfestations in several unrelatedplant species (Szczepaniec et al.2013).

Effects on BirdsGrassland birds are in decline,

and about 25% of species protectedby the Migratory Bird Treaty Act arein trouble. At least 72 million birdsare directly killed by pesticides inthe U.S. each year, and sublethaleffects are probable in 10 timesthat many. So pesticides may beaffecting nearly a billion birds ayear (USFWS 2002; Mineau andPalmer 2013). Organophosphate and carbamate

insecticides often had disastrousand dramatic effects on birds. In1992, when these were in wide-spread use, lethal toxicity frominsecticides was the best predictorof grassland bird decline (Mineauand Whiteside 2013).Neonicotinoids have not resulted

in mass bird killings. But neonicoti-noids may be steadily killing small-er numbers below reportable limits.Kills of less than 200 of a flockingspecies, 50 songbirds, or 5 raptorsdo not have to be reported to theEPA. The major risk is seed treat-ments; one imidacloprid treatedcorn seed, 3-4 cereal seeds, or 4-5canola seeds can be lethal to theaverage bird. About 1/10 of a lethaldose can cause chronic and repro-ductive effects (Mineau and Palmer2013). Seeds are buried by seed drills,

but spills occur, and some birdspecies dig up seeds and plants.Goulson (2013) estimates thataccessible seeds provide enoughpesticide to kill about 20 birds/acre(50/ha). If only 2% of that numberare killed, at least 59 million birdscould be killed by neonicotinoidseach year.The toxicity of neonicotinoids to

birds is underestimated by the EPAdue to neonic species selectivity.There can be a 10-fold difference intoxicity, according to species. Thenorthern bobwhite, Colinus virgini-anus, is not very sensitive to neoni-cotinoids, and that is the speciesthe EPA uses for regulatory deci-sions (Mineau and Palmer 2013).

Effects on Water CreaturesNeonicotinoids are water soluble

and have often been found in sur-face water and groundwater.Starner and Goh (2012) found imi-dacloprid in 89% of water samplestaken from California rivers, creeksand agricultural drains.Concentrations exceeded EPAguidelines in 19% of the cases.Neonicotinoid selectivity may becausing underestimation of theireffects on aquatic creatures.Imidacloprid is 3,800 times moretoxic to Hyalella azteca than to thewater flea, Daphnia magna, used asa test organism by the EPA(Goulson 2013; Mineau and Palmer2013).

ConclusionNeonicotinoids are poisoning

bees, birds and beneficial insectsand polluting water. Though otherinsecticides can also have detrimen-tal effects, neonicotinoid problemsare amplified by the vast amount ofacreage treated. There has been apartial ban in Europe, and the EPAis currently reevaluating neonicoti-noids in the U.S. A temporary banon some uses could give bees,birds, and beneficials time to recov-er while the EPA makes a finaldetermination. Growers would alsobenefit through mitigation of pestresistance, and reduced costs.Where neonicotinoid use is sus-pended, IPM methods can protectcrops.

William Quarles, Ph.D., is an IPMSpecialist, Executive Director of theBio-Integral Resource Center (BIRC),and Managing Editor of the IPMPractitioner. He can be reached byemail, [email protected].

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Bobolink, Dolichonyx oryzivorus,is in decline.

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Home and GardenNeonicotinoids are sprayed on lawns to kill beetle

grubs and other pests. Applications of this type will killbumble bees and soil nesting native bees, and can havean impact on earthworms (Larson et al. 2013). The bestway to avoid spraying neonics on a lawn is to replace itwith native plants or alternative landscaping. Thisapproach is outlined in the BIRC publication,Rethinking the American Lawn (Quarles 2009).One alternative is mowed pathways in native mead-

owgrasses and wildflowers. America is blessed with anumber of strikingly beautiful wildflowers such asCalifornia poppy, Eschscholtzia sp.; black-eyed susan,Rudbeckia spp., purple blazing stars, Liatris spp., andothers. Seed mixtures are available to suit the needs ofyour climate (Daniels 1999). Mowed, gravel, or flag-stone pathways can be integrated with strategicallyplaced raised beds containing vegetables and herbs.Sheet mulching can be used to convert part of yourlawn to planting beds (Quarles 2008a).If you need to keep your lawn, there are cultural

methods and least toxic pesticides to deal with mostlawn pests. Common pests are grubs, billbugs, chinchbugs, cutworms, mole crickets, and sod webworm.Cultural controls such as proper fertilization andwatering; physical controls, such as traps; and biologi-cal controls such as nematodes, Bacillus thuringiensis(BT), and beneficial fungi, can be integrated with least-toxic chemical controls such as neem, insecticidalsoap, natural pyrethrins, and spinosad (Quarles 2006).

OrnamentalsNeonicotinoids are applied as soil drenches and foliar

sprays to protect ornamental shrubs and trees. Foliarsprays can be especially destructive, an example is the

By William Quarles

Neonicotinoids are used on turfgrass and pets, inhome gardens, nurseries, orchards, in structuralpest control, and in commercial agriculture.

Veterinary uses are no threat to wildlife, and structuralpest control applications do not usually threaten bees,birds, and beneficials, as most treatments are appliedinside. However, perimeter sprays applied outside forant control can pollute water, and if applied carelesslyto areas of flowering clover, can kill bees. You can askyour structural pest control company not to useperimeter sprays. You can also take care of ant prob-lems yourself by combining sanitation, exclusion, andant baits (Quarles 2007; Larson et al. 2013).We can protect bees, birds, and beneficials by avoid-

ing pesticides, including neonicotinoids, in a home andgarden situation. We can emphasize cultural practicesthat reduce or eliminate pests, and when pests appear,apply biopesticides or least-toxic materials (Olkowski etal. 2013; Quarles 2013).We can make sure that plants we buy from horticul-

tural nurseries have not been treated with neonicoti-noids. Because these pesticides are systemic, theycould introduce contaminated pollen and nectar intoyour backyard (Hopwood et al. 2012). Much of the neonicotinoid use in the U.S. is on field

crops and in commercial agriculture (Jeschke et al.2011). We can help reduce agricultural use of neoni-cotinoids by buying organic food.To help with bee, bird, and beneficial survival, we can

make intelligent plant choices. If we plant natives whenpossible, choose species that provide pollen and nectarfor bees and beneficials, and plant trees that provideshelter for birds, we can turn our backyard into awildlife paradise. Our local action can have a globaleffect (Quarles 2008b).

Bumble bees, Bombus sp., can be encouraged byplanting floral resources.

From Nixon 1954

Yellow-faced bumble bee, Bombus vosnesenskii

Photo co

urtesy

of G

ary McD

onald

Protecting Bees, Birds, and Beneficials from Neonicotinoids

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1212often used on vegetables such as broccoli (Jeschke etal. 2011). Neonics and other destructive pesticides canbe avoided if you raise your fruit and vegetables organi-cally (Bradley 1995; Ellis and Bradley 1992). Cultural techniques such as companion planting,

incorporation of compost into soil, can be combinedwith physical controls such as traps and row covers,and least-toxic pesticides such as soap and neem. Inemergency situations of aphids and caterpillars, appli-cations of Bacillus thuringiensis (BT), spinosad or natu-ral pyrethrins can help keep pest populations in check(Bradley 1995; Ellis and Bradley 1992; Olkowski et al.2013).

Provide HabitatWe can protect bees, birds, and beneficial insects

from neonicotinoids by providing food, water, and nest-ing sites in our backyards and in crop productionareas. Pollinator protection could easily be added to anumber of existing wildlife conservation programs. The

Humane Society and the Audobon Society both haveUrban Wildlife Sanctuary Programs. There is also BayFriendly Landscaping in the San Francisco Bay Area,the Backyard Wildlife Sanctuary Program inWashington State and others (see Resources). By mak-ing our backyards sanctuaries, we can improve thequality of life for pollinators, urban wildlife and our-selves (NAS 2007).

What to PlantWe can avoid pest problems by choosing the right

plant for the right place and emphasizing native plants.Over a long period of time, native plants have adaptedto the local pests and diseases. When exotic invadersshow up, we can use organic and IPM methods, biopes-ticides and other environmentally friendly approaches(Quarles 2004ab; Olkowski et al. 2013).To increase bee populations, we can increase floral

resources. According to Cane et al. (2008), “in ourcities and towns where most of the native plant com-munities have been displaced by pavement, buildings

50,000 bumble bees killed by dinotefuran sprays onOregon linden trees in 2013 (Black and Vaughn 2013).Neonics are applied in these situations especially for

sucking insects such as aphids, thrips, and whiteflies(Elbert et al. 2008). As an alternative, insecticidal soapand biopesticides can be combined with biological con-trols. Strong streams of water can help dislodge someof these pests (Quarles 2004ab; Olkowski et al. 2013).Predaceous mites are commercially available for thrips,predatory midges eat aphids, parasitoids and predatorsare available for whiteflies. Sources of commercial bio-controls can be found in the BIRC publication IPMPractitioner’s Directory of Least Toxic Pest ControlProducts (BIRC 2013).Systemic neonics also provide some protection for

chewing insects such as caterpillars. BT treatments orspinosad can control these problems. Trees underattack by destructive insects such as the emerald ashborer, Agrilus planipennis, are injected with neonics forsystemic protection. The biopesticide neem is alsoeffective and has fewer destructive effects on bees(Elbert et al. 2008; Hahn et al. 2013; Quarles 2002;Quarles 2005ab; Swiadon and Quarles 2004).

Vegetable GardenNeonics are used as foliage sprays and soil drenches

to protect fruit trees. Foliage sprays of neonics are

California poppy, Eschscholzia californica

Photo co

urtesy

Br. A

lfred Broussea

u

Tidytips, Layia platyglossa

Photo co

urtesy

Gary Monroe

Mason bee, Osmia sp.

Photo co

urtesy

of G

ary McD

onald

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13Common Sense Pest Control XXVIII(1-4) Special Issue 2014 Box 7414, Berkeley, CA 94707

and lawns, our flower gardens can become importantcafeterias of native bees.” Since bees are major pollina-tors, we should give them what they need. Generally,bees need floral sources of nectar and pollen, nestingsites, water, and a pesticide free environment (Black2008). Bees like flowers, sunlight, warm temperatures,and open spaces. Most species prefer to forage whensoil and air temperatures are greater than 55°F(12.8°C). Some limit activity to one, or a few species offlowers, while others such as the honey bee have awide range of hosts (Linsley 1958).Plantings for bee gardens include attractive plants

such as scorpion weed, Phacelia spp.; sunflower,yarrow, mints, borage, bachelor’s button, blackeyedsusan and others (Quarles 2008b). Bee plants can alsoprovide nectar for adult Monarch butterflies, Danausplexippus, that are endangered due to herbicides anddestroyed habitat (Quarles 2011a).

Forage Constantly AvailableSocial bees such as honey bees have perennial

colonies. When foraging plants are not available, theyfeed on stored honey and pollen in the hive. Native beesare driven by the seasons. Solitary bee queens overwin-ter, then establish a nest in the spring. Because theydo not have extensive food stores, forage must be con-stantly available. Floral resources must have overlap-ping flowering periods, so that something is constantlyin bloom (Wojcik et al. 2008). Wildflower seed mixes arecommercially available that can provide forage in openareas (see Resources). Perennials and annuals in plant-ing beds should be chosen with flowering periods inmind. When restoring habitat, native plants are prefer-able because native bees generally prefer native plants(NAS 2007; Frankie et al. 2002; Black 2008).

High Density PlantingWith flower plantings, high density is best for bees.

Frankie et al. (2002) found attraction was increasedwhen large numbers of flowering plants were growingin close proximity. Flowering areas need to be about 1meter (3.2 ft) in diameter to draw in diverse species ofbees. Bees most often seen were the honey bee, Apismellifera; bumble bees, Bombus spp., and leafcutter ormason bees (Megachile spp. and Osmia spp.).

Native Bees, Native PlantsNative bees tend to visit native plants (Schmidt 1980;

Frankie et al. 2002; Schindler et al. 2003). This may bebecause exotics generally produce less pollen and nec-tar than natives. Or perhaps, coevolution of the nativebees and plants caused the preference. Bees attractedvary with the flower species. Bumble bees and sweatbees (Halictidae) often frequent California poppy,Eschscholzia californica. Blackberries attract “a widevariety of leafcutter bees, bumble bees, and honeybees.” Dusty Miller, Centaurea cineraria, attractsmegachilids. Cosmos attracts “large anthophorid beesof the family Apidae” (Frankie et al. 2002). The USDA,and a number of private organizations have produced

lists of flowering plants that function as attractive beegardens (see Resources). A list of plants attractive tonative bees can be found in Tables 1 and 2.

Provide Nesting SitesMost North American native bees nest in the ground.

Sweat bees (Halictidae) and the Adrenidae family digholes in the ground; bumble bees, Bombus spp., like tonest in abandoned rodent burrows. Sunny open hori-zontal areas of well drained soil are preferred, but somespecies nest vertically in banks of soil. Any sunny areain your backyard can be converted to a nesting site byremoving vegetation and mulch (NAS 2007; AAPA1999). About 10% of native bees, such as carpenter bees,

Xylocopa spp., mason bees, Osmia spp., and some leaf-cutters, Megachile spp. nest in wood. Just havingwooden fences can provide sites for twig nesting bees.You can make nests also by drilling 3/16 to 5/16 inch(5 to 8 mm) diameter holes about 4 to 6 inches (10 to15 cm) deep in a 4x4 inch (10 by 10 cm) or 4x6 inch(10 by 15 cm) block of wood. Holes should be 1/4 inch(6 mm) apart. Nest blocks should be attached to postsand trees three to six feet off the ground in areas shad-ed from afternoon sun. Or you can just fill a coffee can,milk carton, or PVC pipe other container with drinkingstraws 1/4 to 3/8 inches (6 to 9.5 mm) diameter.Entrance holes should be placed horizontal, and thenests should be protected from rain (NAS 2007; AAPA1999; Greer 1999).

Avoid PesticidesWe should avoid not only neonicotinoids, but other

pesticides. Pollinators such as bees, and other benefi-cial insects such as ladybugs, lacewings, and parasiticwasps are easily killed by insecticides. For a number ofreasons, beneficials are more vulnerable to insecticidesthan are insect and mite pests (Croft 1990). Herbicides

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Bumble bee nest. Spheres are cocoons containingbee larvae. Open cocoons in the center are usedfor storing honey.

From Nixon 1954

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can destroy flowering plants that otherwise feed polli-nators. Chemical fungicides are often synergistic withinsecticides, and combinations are especially lethal tobees. Cultural methods and microbial fungicides areless damaging alternatives (Quarles 2008ab; 2004ab;2005ab; 2013).When possible, chemical pesticides should be avoided

altogether by growing organic gardens, lawns, andlandscapes, and switching to organic farm production.(Note: There are many articles about alternatives topesticides listed on the BIRC website at www.birc.org).Insecticides should not be applied while a crop is inbloom or while bees are foraging. Some applicationtimes are better than others. Night applications arebest, as bees are not foraging. However, favorable application times depend on the

species. Early morning applications that spare honeybees will kill bumble bees out for a morning snack.Bumble bees and other ground nesters are also more atrisk from pesticides such as imidacloprid and clothiani-din applied to lawns and turf for grub control (NAS2007; Schacker 2008). Many microbial pesticides can be used safely with

bees. Microbial pesticides have such low toxicity, thathoney bees have been used to apply Bacillus subtilisand Beauveria bassiana in organic cropping situations.Targeted insecticides such as Bacillus thuringiensis(BT), Chromobacterium sp., and least toxic insecticidessuch as soaps, oils, or quickly degraded botanicalsminimize damage to pollinators. Though BT might havean impact on the larval form of butterflies, it is usuallyapplied to plants that butterflies do not utilize (NAS2007; Quarles 2004ab; Quarles 2006; Quarles 2013).

Plants for BirdsBirds need trees and shrubs for shelter. Plants that

provide seeds, berries, or fruit are also attractive.Sunflower, Helianthus sp.; Cosmos sp., purple cone-flower, Echinachea sp., manzanita, Arctostaphlos sp.,crabapple, Malus sp., elderberry, Sambucus sp.,cotoneaster, and blackberry are attractive to birds.Extensive lists can be found on the internet and helpfuladvice can be found at your local horticultural nursery(Roth 1998; Adams 1998).

Insectary Plants for BeneficialsProtecting pollinators has many rewards. Many of the

same plants that feed pollinators such as bees, birdsand butterflies will also provide refuge for biocontrolagents such as ladybugs and lacewings. You can haveboth better pollination and fewer pests feeding on yourgarden. Insectary plants used to conserve beneficialinsects include native annual wildflowers such asCalifornia poppy, Eschscholzia californica; buckwheat,Eriogonum; and tansy leaf, Phacelia tanacetifolia. Otherpossibilities include umbelliferous herbs such ascoriander, chervil, and fennel, garden flowers such assweet alyssum, Lobularia maritima; yarrow, Achilleamillefolium; baby blue eyes, Nemophila and tidy tips,Layia platyglossa (Quarles and Grossman 2002). Sweet

alyssum and phacelia have so much pollen, they areplanted in organic lettuce fields to attract syrphid fliesfor aphid control (Chaney 2007). Perennials such as California lilac, Ceanothus spp.;

yarrow, Achillea millefolium; coyote bush, Baccharispilularis; and perennial grasses are also good foodsources. These plantings have something in bloom allyear, so native bees and beneficials have a constantfood supply (Long et al. 1998).

Roadside Restoration and Vacant LotsSeed mixes containing native plants such as black-

eyed Susan, Rudbeckia hirta; butterfly weed, Asclepiastuberosa; bergamot, Monarda sp., and similar plantscompete with weeds along roadsides, reducing herbi-cide applications (see Resources). Wildflowers used in

these mixes also increase biocontrol and provide foragefor migrating butterflies (Quarles 2003). For instance,roadside native plantings in Iowa showed a 5-foldincrease in butterfly abundance. Native plants alsocrowded out weeds and reduced the number of cornborers, Ostrinia nubilialis in nearby cornfields (Quarles2003; Harper-Lore and Wilson 2000; Ries et al. 2001).Roadsides restored with native plants in Iowa had

greater numbers of native bees and greater bee diversi-ty. Nearby traffic did not bother the bees. Most impor-tant were the floral resources and availabilty of groundnesting sites. There are millions of acres along road-sides that could be used to support native bees. Thevegetation planted could also improve roadside weedmanagement (Harper-Lore and Wilson 2000; Hopwood2008).Plantings of milkweed, Asclepias spp., should be

included in roadside restoration. The milkweed habitatfor the Monarch butterfly, Danaus plexippus, has beendestroyed by overuse of herbicides (Quarles 2011a).Vacant lots should also be seeded with wildflower

mixes and milkweed. If owners are contacted, theyshould be happy to help reduce blight in urban areas.

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Populations of Monarchs, Danaus plexippus, haveseen massive losses, partly due to pesticides.

Photo co

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Flowering buckwheat,Eriogonum sp.

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16 Box 7414, Berkeley, CA 94707Common Sense Pest Control XXVIII(1-4) Special Issue 2014

Commercial OrchardsNeonicotinoids are applied as foliage sprays and soil

drenches in orchards. As an alternative, biopesticides,pheromone mating disruption, and insect growth regu-lators can be used. Cultural methods, such as the useof cover crops, can be employed (Flint and Roberts1988; Quarles 2013).

Field CropsNeonicotinoid seed treatments are used on most of

U.S. row crops such as corn, soybeans, canola, andsunflowers (Jeschke et al. 2011). Seed treatments arethe latest manifestion of the pesticide treadmill result-ing from agribusiness farming—vast fields of unsus-tainable monocultures supported by genetically modi-fied plants, synthetic fertilizers, pesticidal seed treat-ments, and massive use of glyphosate and other herbi-cides. IPM methods have been abandoned, not becausethey are ineffective or less profitable, but becauseagribusiness has convinced farmers that this approachis simpler and less labor intensive (Kremen et al. 2002;Gray 2011, Pimentel et al. 2005; Liebman et al. 2008,Quarles 2011a).Fungicidal seed treatments are needed because aerial

sprays of glyphosate on GMO crops are encouragingplant disease. If a farmer is already using fungicidalseed treatments, adding insecticides to the mix adds tocost, but not to labor. Often, neonicotinoids are notneeded, and may not increase yields (Johal and Huber2008, Seagraves and Lundgren 2012).

Break Up MonoculturesLarge monocultures cause many of the problems

associated with conventional agriculture. Extensiveunbroken acreage of the same crop, such as corn orcotton, encourages arthropod pests (insects and mites)that specialize in these crops (Root 1973; Elton 1958;Andow 1991). Because pest populations expand morerapidly than beneficial populations in these situations,broad-spectrum pesticides are applied. These pesticides

then cause problems such as target pest resistance,pest resurgence, and secondary pest outbreaks that areall too familiar (DeBach and Rosen 1991). Monocultures can be replaced by intercropping,

hedgerow plantings, and plant diversity. Diversity canbe introduced into a field by stands of flowering insec-tary plants (Bugg et al. 1998; van Emden 1962; vanEmden 1965), encouraging flowering weeds at fieldboundaries (Nentwig 1998; Bugg et al. 1987) plantingcover crops (Bugg et al. 1996), or simply rotating cropsin smaller fields so that each field is always adjacent toa different and complementary crop (Altieri 2004).

Say it with Flowers As we saw above, home gardens can benefit from

planting of floral resources that feed bees and benefi-cial insects. Bees and beneficials can also be nurturedand encouraged through field plantings of flowers con-taining abundant pollen and nectar (Bugg et al. 1998).Yellow flowers and plants such as tansy leaf, Phaceliatanacetifolia, are particularly attractive to syrphids (vanEmden 1965; White et al. 1995). Native annual wildflowers, buckwheat, Eriogonum sp.;

toadflax, Linaria sp.; umbelliferous herbs such ascoriander and chervil, and garden flowers such assweet alyssum, Lobularia maritima; baby-blue-eyes,Nemophila sp.; and tidy-tips, Layia platyglossa allattracted numerous beneficial braconid wasps, ladybeetles, pirate bugs, spiders and other natural enemies(Quarles and Grossman 2002).White sweet alyssum has been used to protect

against aphids in California lettuce fields. parasiticwasps are attracted by plentiful, small flowers whichprovide easy feeding for the tiny beneficials (Chaney1998; Altieri 2004).

Hedgerow PlantingsHedgerows can provide shelter from the wind, barri-

ers to pest invasion, and food and shelter for beneficialinsects, birds, and bees. As well as annuals, perennialspecies can provide food sources and habitat for bees,

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Wild sunflower, Helianthus sp.

Photo co

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White rows of flowering alyssum, Lobularia maritima,feed beneficial insects that provide biocontrol.

Photo co

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illiam Chaney

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17Common Sense Pest Control XXVIII(1-4) Special Issue 2014 Box 7414, Berkeley, CA 94707

birds, and beneficials. In California, hedgerows about 3m (9.8 ft) wide along field margins have been plantedwith common yarrow, Achillea millefolium; coyote bush,Baccharis pilularis; elderberry, Sambucus mexicana;California lilac, Ceanothus griseus; perennial buck-wheat, Eriogonum giganteum; toyon, Heteromeles arbuti-folia, and coffee berry, Rhamnus californica. Perennialgrasses included, purple needlegrass, Nassella pulchra,California melic, Melica californica; blue wildrye,Elymus glaucus; and creeping wildrye, Leymus triti-coides (Long et al. 1998; Bugg et al. 1998). Larger populations of beneficials are found in fields

with hedgerows rather than weedy field margins. About78% of insects found in hedgerows are beneficials.Beneficials also travel into crops to provide biologicalcontrol (Pisani-Gareau et al. 2013; Morandin et al.2011; Long et al. 1998; Bugg et al. 1998).

Close to HomeSince neonics are systemics, they appear in food.

According to the USDA Pesticide Data Program, imida-cloprid was detected in about 36% of lettuce samplestested, 26% of sweet bell peppers, and 20% of cherrytomatoes. Acetamiprid was found in 26%, and thiaclo-prid was found in 13% of baby food pears; thiamethox-am in 17% of hot peppers; dinotefuran in 12% of can-taloupes (USDA 2011).By protecting bees, birds and beneficials from neoni-

cotinoids and other pesticides and buying organic food,we will be protecting ourselves.

William Quarles, Ph.D., is an IPM Specialist, ExecutiveDirector of the Bio-Integral Resource Center (BIRC), andManaging Editor of the IPM Practitioner. He can bereached by email, [email protected].

ReferencesAAPA (American Association of Professional Apiculturists). 1999. Bee

Pollinators in Your Garden. AAPA Technical Bulletin No. 2,Entomology Department, University of California, Davis, CA. 19 pp.

Adams, G. 1998. Birdscaping Your Garden. Rodale Press, Emmaus, PA.208 pp.

Andow, D.A. 1991. Vegetational diversity and arthropod populationresponse. Annu. Rev. Entomol. 36:561-86.

Altieri, M.A. 2004. Agroecology and sustainable agriculture. IPMPractitioner 26(9/10):1-7.

BIRC. 2013. IPM Practitioner’s 2013 Directory of Least-Toxic Pest ControlProducts. Bio-Integral Resource Center, PO Box 7414, Berkeley, CA94707. 52 pp. www.birc.org

Black, S.H. 2008. Native pollinators: how to protect and enhance habi-tat for native bees. Native Plants J. 9(2):80-91.

Black, S.H. and M. Vaughn. 2013. Pesticide causes largest mass bum-ble bee death on record. The Xerces Society for InvertebrateConservation. www.xercessoc.org

Bradley, F.M. 1995. Rodale’s Garden Answers: Vegetables, Fruits, andHerbs. Rodale Press, Emmaus, PA. 374 pp.

Bugg, R.L., L.E. Ehler and L.T. Wilson. 1987. Effect of commonknotweed on abundance and efficiency of insect predators of croppests. Hilgardia 55:1-51.

Bugg, R.L., G. McGourty, M. Sarrantonio, W.T. Lanini and R.Bartolucci. 1996. Comparison of 32 cover crops in an organic vine-yard on the north coast of California. Biol. Agric. Hort. 13(1):63-81.

Bugg, R.L., J.H. Anderson, C.D. Thomsen and J. Chandler. 1998.Farmscaping in California. In: Pickett and Bugg, pp. 339-374.

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Flowering Plant Lists and SeedsCornflower Farms, www.cornflowerfarm.comNative American Seeds, www.seedsource.comPlants Attractive to Native Bees, USDA,

http://www.ars.usda.gov/research/docs.htm?docid=12052

Selecting Plants for Pollinators, Pollinator Partnership,http://www.pollinator.org

Urban Bee Gardens, University of California, Berkeley,http://nature.berkeley.edu/urbanbeegardens/

Wildflower Farm, www.wildflowerfarm.comXerces Society Seeds, www.xercessociety.org/pollinator-

seed

OrganizationsAmerican Bird Conservancy, www.abcbirds.orgAudobon Society, www.audobon.orgAmerican Association of Professional Apiculturists,

www.masterbeekeeper.orgBackyard Wildlife Sanctuary Program,

http://wdfu.wa.gov/living/backyardBay Friendly Gardening, www.bayfriendlycoalition.orgCalifornia Native Plant Society, www.cnps.orgGolden Gate Audobon, www.goldengateaudobon.orgHumane Society, Backyard Sanctuary Program,

www.hsus.orgNational Wildlife Federation, www.nwf.orgNorth American Butterfly Association, www.naba.orgNorth American Pollinator Protection Campaign,

www.nappc.orgPollinator Partnership, www.pollinator.orgXerces Society, www.xerces.org

Monitoring and Identifying PollinatorsBee Identification,

http://www.discoverlife.org/20/q?search=ApoideaMonitoring bees, http://online.sfsu.edu/~beeplot/Monitoring butterflies, www.monarchwatch.orgMonitoring birds, Audobon Society Christmas Bird

Count,http://audubon2.org/birds/cbc/hr/graph.html;Breeding bird survey, http://www.mbr-pwrc.usgs.gov/bbs/bbs.html

Bees and EquipmentSweep Nets, Bee Collection Materials—BioQuip Products,

2321 Gladwick Street, Rancho Dominguez, CA 90220;310/667-8800, Fax 310/667-8808; www.bioquip.com

Beekeeping Equipment—Dadant & Sons, 51 S. 2nd St.,Hamilton, IL 62341-1399; 888/922-1293, 217/847-3324, Fax 217/847-3660; www.dadant.com

Honey bees—Brushy Mountain Bee, 610 Bethany ChurchRd., Moravian Falls, NC 28654; 800/233-7929;Draper’s Super Bee Apiaries, RR#1, Box 97, Millerton,PA 16936; 800/233-4273; Glorybee, 120 N. SenecaRd., Eugene, OR 97402; 800/456-7923

Bumble bees—Hydro-Gardens, Inc., PO Box 25845,Colorado Springs, CO 80936; 800/634-6362,719/495-2266, Fax 719/495-2266; www.hydro-gar-dens.com

Mason bees—Knox Cellars, 25724 NE 10th St., Redmond,WA 98053; 425/898-8802; www.knoxcellars.com

Mason bees and leafcutters—International PollinationSystems, 16645 Plum Road, Caldwell, ID 83605;800/990-1390; www.pollination.com.

Resources

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Cane, J.H., L.Kervin, R. Thorp, T.Miklasiewicz and L. Day. 2008. Gardeningfor native bees in North America.USDA/ARS,www.ars.usda.gov/mian/docs.htm?docid=12050

Chaney, W.E. 1998. Biological control ofaphids in lettuce using in-field insectaries.In: Pickett and Bugg, pp. 73-83.

Chaney, W. 2007. Organic lettuce biocontrol.IPM Practitioner 29(5/6):9-10.

Croft, B.A. 1990. Arthropod Biological ControlAgents and Pesticides. John Wiley andSons, New York. 723 pp.

Daniels, S., ed. 1999. Easy Lawns: LowMaintenance Native Grasses for GardenersEverywhere. Brooklyn Botanic Garden,Brooklyn, NY. 111 pp.

DeBach, P. and D. Rosen. 1991. BiologicalControl by Natural Enemies, 2nd. ed.Cambridge University Press, New York.

Elbert, A. M. Haas, B. Springer et al. 2008.Applied aspects of neonicotinoid uses incrop protection. Pest Manag. Sci. 64:1099-1105.

Ellis, B.W. and F.M. Bradley. 1992. TheOrganic Gardener’s Handbook of NaturalInsect and Disease Control. Rodale Press,Emmaus, PA. 534 pp.

Elton, C.D. 1958. The Ecology of Invasions byAnimals and Plants. Methuen, London.[cited in Andow 1991]

Flint, M.L. and P.A. Roberts. 1988. Using cropdiversity to manage pest problems: someCalifornia examples. Am. J. AlternativeAgric. 3(4):163-167.

Frankie, G.W., R.W. Thorp, M.H. Schindler, B.Ertter and M. Przybylski. 2002. Bees inBerkeley? Fremontia 30(3/4):50-58.

Frankie,G.W., R.W. Thorp, R. Coville, M.Schindler, B. Ertter, J. Hernandez, J.Pavelek and S. Witt. 2008.Urban BeeGardens, http://nature.berkeley.edu/urbanbeegardens/

Gray, M.E. 2011. Relevance of traditional inte-grated pest management (IPM) strategiesfor commercial corn production in atransgenic agroecosystem—a bygone era?J. Agric. Food Chem. 59:5852-5858.

Greer, L. 1999. Alternative pollinators: nativebees. ATTRA Horticulture Tech. Note. 12pp.

Hahn, J., D.A. Herms and D.G. McCullough.2013. Frequently asked questions regard-ing potential side effects of systemics usedto control emerald ash borer. CooperativeExtension, Univ. Minnesota, MichiganState, and Ohio State. 4 pp.

Harper-Lore, B.L. and M. Wilson. 2000.Roadside Use of Native Plants. IslandPress, Washington, DC. 665 pp.

Hopwood, J., M. Vaughan, M. Shepherd, D.Biddinger et al. 2012. Are NeonicotinoidsKilling Bees? The Xerces Society forInvertebrate Conservation. 33 pp.www.xercessoc.org

Hopwood, J., S.H. Black, M. Vaughn and E.Lee-Mader. 2013. Beyond the Birds andthe Bees. The Xerces Society forInvertebrate Conservation. 25 pp.www.xercessoc.org

Hopwood, J.L. 2008. The contribution of road-side grassland restorations to native beeconservation. Biol. Conservation141(10):2632-2640.

Jeschke, P., R. Nauen, M. Shindler and A.

Elbert. 2011, Overview of the status andglobal strategy for neonicotinoids. J. Agric.Food Chem. 59:2897-2908

Johal, G.S. and D.M. Huber. 2009.Glyphosate effects on diseases of plants.Eur. J. Agron. 31:144-152.

Kremen, C., N.M. Williams and R.W. Thorp.2002. Crop pollination from native bees atrisk from agricultural intensification. Proc.Natl. Acad. Sci. USA 99:16812-16816.

Larson, J.L., C.T. Redmond and D.A. Potter.2013. Assessing insecticide hazard tobumble bees foraging on flowering weedsin treated lawns. PLoS ONE 8(6):e366375

Long, R.F., A. Corbett, C. Lamb, C.R.-Horton,J. Chandler and M. Stimmann. 1998.Beneficial insects move from floweringplants to nearby crops. Calif. Agric.52(5):23-26.

Liebman, M., L.R. Gibson, D.N. Sundberg etal. 2008. Agronomic and economic per-formance characteristics of conventionaland low external input cropping systemsin the central Corn Belt. Agronomy J.100:600-610.

Linsley, E.G. 1958. The Ecology of SolitaryBees. Hilgardia 27(19):543-585.

Morandin, L., R.F. Long, C. Pease and C.Kremen. 2011. Hedgerows enhance bene-ficial insects on farms in California’sCentral Valley. Calif. Agric. 65(4):197-201.

NAS (National Academy of Sciences). 2007.Status of Pollinators in North America.National Academy Press, Washington, DC.300 pp.

Nentwig, W. 1998. Weedy plant species andtheir beneficial arthropods: potential formanipulation in field crops. In: Pickettand Bugg, pp. 49-67.

Nixon, G. 1954. The World of Bees.Hutchinson, London. 214 pp.

Olkowski, W., S. Daar and H. Olkowski. 2013.Gardener’s Guide to Common Sense PestControl. 2nd ed. S. Ash, ed. TauntonPress, Newtown, CT.

Pickett, C.H. and R.L. Bugg, eds. 1998.Enhancing Biological Control. University ofCalifornia Press, Berkeley. 422 pp.

Pimentel, D., P. Hepperly, J. Hanson et al.2005. Environmental, energetic, and eco-nomic comparisons of organic and con-ventional farming systems. BioScience55:573-582.

Pisani-Gareau, T.L., D.K. Letourneau and C.Shennan. 2013. Relative densities of nat-ural enemy and pest insects withinCalifornia hedgerows. Environ. Entomol.42(4):688-702.

Quarles, W. and J. Grossman. 2002. Insectaryplants, intercropping, and biological con-trol. IPM Practitioner 24(3):1-11.

Quarles, W. 2002. The urban forest in yourbackyard. Common Sense Pest ControlQuarterly 18(3):3-6.

Quarles, W. 2003. Native plants and integrat-ed roadside vegetation management. IPMPractitioner 25(3/4):1-9.

Quarles, W. 2004a. Non-toxic fungicides forroses. Common Sense Pest ControlQuarterly 20(3):6-15.

Quarles, W. 2004b. Sustainable urban land-scapes and integrated pest management.IPM Practitioner 26(7/8):1-11.

Quarles, W. 2005a. Neem protects ornamen-tals in greenhouses and landscapes. IPMPractitioner 27(5/6):1-14.

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Quarles, W. 2005b. Spinosad finds a home inorganic agriculture. IPM Practitioner27(7/8):1-9.

Quarles, W. 2006. IPM for turfgrass insectpests. Common Sense Pest ControlQuarterly 22(1):3-11.

Quarles, W. 2007. IPM for the Argentine ant.Common Sense Pest Control Quarterly23(2/3):8-20.

Quarles, W. 2008a. Mulch optimization inintegrated pest management. IPMPractitioner 30(7/8):1-10.

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Quarles, W. 2009. Rethinking the Americanlawn. Common Sense Pest ControlQuarterly 25(1):3-10.

Quarles, W. 2011a. Brave new world: systemicpesticides and genetically engineeredcrops. IPM Practitioner 33(3/4)1-9.

Quarles, W. 2011b. Pesticides and honey beedeath and decline. IPM Practitioner33(1/2):1-8.

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Schacker, M. 2008. A Spring Without Bees.The Lyons Press, Guilford, CT. 292 pp.

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Seagraves, M.P. and J.G. Lundgren. 2012.Effects of neonicotinoid seed treatmentson soybean aphid and natural enemies. J.Pest. Sci. 85:125-132.

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Wojcik, V.A., G.W. Frankie, R.W. Thorp andJ.L. Hernandez. 2008. Seasonality in beesand their floral resource plants at a con-structed urban bee habitat in Berkeley,CA. J. Kans. Ento. Soc. 81(1):15-28.

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Dear BIRC Members

Decreased income has forced usto reduce the number ofQuarterly issues that we produceeach year. This Special Issue willbe the only Quarterly producedin 2014. Quarterly Members willalso receive three issues of ourother publication—the IPMPractitioner.

We appreciate your support, andhope you will continue as BIRCmembers.

Thank you,William Quarles, Ph.D.Executive Director

AcknowledgementBIRC wishes to thank the JiJi Foundation for a generous grantthat helped with production of thispublication.

Page 20: Neonicotinoids, Bees, Birds and Beneficial Insects · Bumble bees and other native bees are also dying (Whitehorn et al. 2012). Part of the problem is expo-sure to systemic insecticides