<<

A Decision Making Guide to Protect Pollinators in Tree Fruit Orchards

2020 Edition Maria van Dyke, Emma Mullen, Dan Wixted, and Scott McArt Notes Notes Pollinator Network at Cornell, 2020 Cornell University, Department Of Entomology

Contents

Choosing lower-risk for pollinators in New York orchards 1 How to use this guide 3 Understanding the terms in this guide 4 EPA Pesticide toxicity standards 4 Synergistic Interactions 4 Systemic Pesticides 4 Adjuvants and/ inert ingredients 5 Tying it all together: adopting an Integrated Pest and Pollinator Management (IPPM) approach 5 IPPM: Putting the “pollinator” in IPM: 6 Table 1: Product formulations and their active ingredients 7 Table 2: Pesticide synergies and acute, chronic, and sublethal toxicities for honey and other pollinators 9 Part A: including antibiotics for use on tree fruit ______9 Part B: Mixtures of fundicides and for use on tree fruit ______15 Part C: Insecticides including insect growth regulators for use on tree fruit ______16 Part D: Adjuvants, stickers, inert ingredients, and registered synergists used in formulations_ 23 Literature cited 24 Appendix A: Pollination contract ______29

Acknowledgments This research and development of this guide was supported by the New York State Environmental Protection Fund and New York Farm Viability Institute grant FOC 17-001. The expert advice and consultation provided by Dan Wixted of the Cornell Pesticide Management Education Program was supported by the Crop Protection and Pest Management Extension Implementation Program [grant no. 2017-70006-27142/project accession no. 1014000] from the USDA National Institute of Food and Agriculture. Choosing lower-risk pesticides for pollinators in New York orchards Growers recognize the vital role of pollination and understand that managing pests while protecting pollinators can be a balancing act. Both components are essential for a successful harvest, yet they can sometimes be in conflict with one another. Pollinators (mostly bees) are busy pollinating flower blossoms at the same time growers need to be managing specific pests and diseases. The impact of pesticides on pollinator health has been an active area of research in recent years, including work conducted in agricultural fields and urban and natural habitats, including New York apple orchards. The results from this research are clear: Some pesticides can be a threat to pollinators, but there is variation in risk, due in part to grower management practices. This guide summarizes impacts of pesticides on bees in a clear, concise, easy-to-use format. Our goal is to provide information to growers so they can develop an effective Integrated Pest and Pollinator Management program. esticide risk to pollinators comes from a combination of exposure and effects. Pollinators may be exposed to pesticides through direct sprays, puddle water, guttation droplets, extrafloral nectaries, pollen and nectar from treated crops and surrounding wildflowers, and residues that accumulate in soil (for ground nesting bees) and in nesting materials (for example leaves for leaf-cutter bees). Pesticides have an effect on pollinators if exposure is sufficient to cause lethal or

sub-lethal impacts. Pesticides can directly C Kitchen kill pollinators, reduce offspring © production, or have more subtle effects A native Andrena species grooming cherry pollen from its face. on body size or behavior. Recently, an understanding of the interactions between pesticides on health has brought focus on active ingredients that synergize, meaning that the combined toxicity is greater than the sum of the toxicity of each pesticide applied separately. Pesticide risk studies find that synergies among different pesticides can increase the toxicity of some pesticides up to 1000-fold. While some synergies are intentional and make a higher efficacy formulation for the pests they are meant to control, many synergies can lead to unintentional combined effects that can substantially increase pesticide risk to bees. These synergies are beyond the scope of EPA label guidelines, which is why we chose to share the information in this guide. In summary, 47 of the 140 chemicals listed in this guide have been shown to synergize with other agrochemicals in tank mixes, formulations, or on plant or soil surfaces. These chemicals include some fungicides, , , , organophosphates, piperonyl butoxide and some adjuvants. Synergisms are noted with a in Table 2, ‘Synergies and acute, chronic, and sublethal toxicities for honey bees and other pollinators.’

1 This guide summarizes reported pesticide effects as of April 2020. The guide presents the most up-to- date information about the impacts of the fungicides, insecticides, microbicides, and growth regulators on bees that pollinate tree fruits. New York is home to 416 species of bees, and over 120 species are known to be important for NYS apple pollination, with several of those species also visiting other tree fruits. It is well documented that each bee Honey bee species can respond differently to active ingredients. KL However, there are so many bee species, each © differing with respect to physiology, sociality, nesting habits, foraging habits, and ability to tolerate pesticides, that it is unrealistic to determine how every use of every pesticide will affect each species. Therefore, the Environmental Protection Agency (EPA) generally uses acute toxicity to honey bees (Apis mellifera) as a proxy for the potential adverse effects of a pesticide on bees in general, but will at

times take studies on other bee species into account

Mining bee KL

as appropriate. In addition to presenting these EPA © toxicity ratings, this guide specifically highlights the chemical combinations that produce synergistic effects on bee pollinators. Furthermore, we expand on EPA standards to include reports of sublethal effects in honey bees as well as acute, chronic, and sublethal effects on bumble bee and solitary bee species. Chronic and sublethal effects include reduced reproduction, size, immunity, and negative effects on bee behaviors such as cleaning, nesting, Cellophane bee foraging, and flying (Table 2, last column). C Kitchen © This guide is intended to be used as a decision-making tool. The primary goal of this guide is to help growers understand and compare the acute toxicity and synergistic effects of different pesticides on pollinators. The majority of registered products for New York orchard management are included and EPA ratings of “highly toxic”, “moderately toxic”, or “practically non-toxic” are noted by color coding in Table 2. In addition information on synergies, sublethal effects and effects on bee species other than honey bees are noted in the last column. If growers are in a situation where multiple chemical tools could be effective against pests, then this guide will allow them to easily compare the toxicity ratings of various pesticides to help them choose a product that poses minimal risk to bees. The Pollinator Network @ Cornell will update this guide as new research is published. This guide is intended to be a companion to the Cornell Pest Management Guide for Commercial Tree Fruit Production.

2 How to use this guide This guide consists of a series of tables that summarize all the known products and their associated active ingredients used in orchard production. It also includes miticides that are used by beekeepers in New York. Growers and applicators can most effectively use this guide by following three steps: 1. Locate specific pesticide products in Table 1 to determine the product’s active ingredients. 2. Go to Table 2 to find active ingredient toxicity ratings and known synergisms. 3. When possible, choose to apply products that are effective on target pests but least toxic to bees and do not synergize with other products used. Table 1: Product formulations and their active ingredients This table lists most but not all registered vegetable pesticides, in New York, alphabetically by product name so it’s easy to find the associated active ingredient. If a product name is not in this product formulation list, please be aware that the active ingredient is always listed on the product label. Information on toxicity and synergy is organized by active ingredient in Table 2. ©Emma Mullen Table 2: Synergies and acute, chronic, and sublethal toxicities for honey bees and other bee species This table lists all the active ingredients alphabetically, noting EPA honey bee guidelines for acute contact toxicity ratings, ability to synergize, chronic effects, sublethal effects, and/or impacts to non- honey bee pollinators. Pesticides are grouped in this table according to class: A: Fungicides, antibiotics, and inert ingredients, B: Mixtures of insecticides and fungicides, C: Insecticides including insect growth regulators, and D: Synergists, adjuvants and inert ingredients. In the 3rd to 5th columns of this table, the EPA’s acute toxicity ratings for adult honey bees are reported, and the symbol is added if a synergy has been documented. Notes on the active ingredients that cause synergistic interactions, as well as information on sublethal impacts or impacts to other bee species are outlined in the 6th column. Timing of spray is typically noted on the label. Applicators are to use the most conservative timing when a potentially synergistic combination must be used. While this guide has highlighted all laboratory and experiments that have measured synergies beween active ingredients, and the sublethal, chronic, and developmental impacts of pesticides to honey bees (Apis mellifera) and other bee species, it is not an exhaustive list of all product formulations or all pesticides used in agriculture. The toxicity ratings in columns 3-5 of this guide refer to current registration standards set forth by the EPA based on acute toxicity of pesticides to adult ©C Kitchen honey bees. Where additional considerations for other bee Bombus impatiens on a cherry flower. species are known from scientific literature, including chronic toxicity, sublethal toxicity, or larval or pupal toxicity, we have reported these risks in the ‘Pesticide synergies, sublethal effects, and toxicity to bee species other than the honey bee in vegetable crops’ column in Table 2.

3 Understanding the terms in this guide Pesticide toxicity (i.e. acute, sublethal) Toxicity of pesticides is based on oral and/or contact exposure, honey bee caste, and time periods of exposure. At present, the EPA guidelines have standardized toxicity testing to acute contact exposure with a one-time dose over 4, 24, 48, and if applicable, 96 hours. Acute contact toxicity is the dose or concentration of an active ingredient that it takes to kill 50% of adult worker honey bees that are exposed within 48 hours. The lethal dose of an ingredient is referred to as the LD50 value. Acute pesticide toxicity is grouped into three categories: highly toxic (LD50 < 2 μg/bee), moderately toxic (LD50 2 - 10.99 μg/bee) practically non-toxic (LD50 > 11 μg/bee)

The EPA is currently working to adjust their registration standards to address risk, which consolidates toxicity data with exposure predicted from field application rates. These risk rankings will be available in a few years and, when they are, will be included or referenced in a future edition of this guide. Synergistic Interactions Traditionally, pesticide toxicity evaluates one active ingredient at a time. With our growing understanding of the multitude of pesticides bees come into contact with simultaneously, we now know that the overall risk posed to bees in the environment is tied to how mixtures of pesticides interact with one another. Some pesticides commonly used in orchard management have been identified as synergists (see Table 2). Certain classes of fungicides and adjuvants are commonly reported to synergize with insecticides to create greater than expected effects on bees. For instance, the combination of DMI fungicides (e.g. myclobutanil, difenoconazole, propiconazole) with some pyrethroids or neonicotinoids have been found to create these effects. This guide highlights active ingredients that are known synergists and the mixtures that should be avoided whenever possible to mitigate risk to bees. This information is especially helpful when planning tank mixes and spray regimes. Keep in mind that the conditions for synergy can vary depending on formulation, weather, and time since application of an active ingredient. While we understand that tank mixing is a cost-effective and time-saving practice, we encourage applicators to identify and avoid certain pesticide combinations that are likely to cause synergisms (Table 2). Systemic Pesticides “Systemic” pesticides are able to protect the entire plant instead of one isolated part of the plant. The pesticide is translocated within the plant from the point of uptake to the The life cycle of a solitary ground nesting bee. Bees are exposed to petals, leaves, stem, roots, pesticides in soil and in the pollen and nectar they consume as larvae. pollen and nectar to protect Photos by Laura Russo.

4 the plant from a variety of pests. Unfortunately, this also means that these pesticides can be present in pollen, nectar, and guttation droplets for days or weeks, which can result in exposure to pollinators. The most common systemic pesticides are the neonicotinoids (, , , , nitenpyram, , ) and , a phenylpyrazole . A real conundrum we face is that it is legal to plant seeds coated in systemic pesticides not registered in NY (e.g. clothianidin). As a systemic, bees can consume chemicals when they forage on the nectar and pollen at bloom time, resulting in exposure and increasing the potential for synergy. Applicators often need to spray fungicides on plants treated with systemics-- increasing the potential for synergy when bees forage. Some neonicotinoids can persist in the soil for years and be taken up by nearby plants at any time creating a high likelihood for bee exposure and potential to synergize with other pesticides. Adjuvants and/or inert ingredients Adjuvants are chemicals added to a pesticide spray mix to improve performance. Inert ingredients are chemicals in a pesticide product formulation aside from the active ingredient(s). The literature on this topic is young, so we have included only a handful of these chemicals in Table 2 because recent findings have demonstrated that inerts and adjuvants are highly toxic to bees (for example, N-methyl-2- pyrrolidone and organosilicones).

Tying it all together: adopting an Integrated Pest and Pollinator Management (IPPM) approach to protect pollinators Growers and pesticide applicators have already made marked adjustments for the protection of bees by following pesticide label guidelines. Pesticide labels inform users about bee precautions in a “Bee Advisory Box”, in the “Directions for Use” section, and/or in the “Environmental Hazards Statement” section of the product label. These precautions include information about the time, temperature, and Spraying in low-wind conditions can reduce drift,©van Dyke wind speeds under which pesticides can be especially when using a typical airblast sprayer. safely applied, and may specify additional requirements for reducing drift. Whether growers work closely with a county extension educator, a crop consultant, or a distributor, they must always read the pesticide label carefully. When reading the label, always note guidelines for each crop, the proper mixing rate, the proper method of application, and the proper timing (e.g., weather conditions, time of day, stage of bloom) for minimizing negative impacts on non-target organisms and humans. Check active ingredient name(s) and their compatibility in Table 2 with other a.i.’s that will be applied at the same time and in the same tank mix. Take a whole farm approach and consider what is currently being sprayed on all of your crops at the same time. Bees may visit these fields to collect pollen and be exposed to a differing pesticide

5 mix before they arrive in your focal field creating the potential for two synergizing active ingredients from two different fields being brought together in a single pollen provision. While this is difficult to avoid, strict adherence to timing and drift instruction on the label may help. Growers can verify currrent registration of products for use in their state. In New York, product registration is confirmed on the New York State Pesticide Administration Database (NYSPAD): http://www.dec.ny.gov/nyspad/. If growers are using this guide in another state, they should check with their own state’s pesticide registration program/database or the National Pesticide Information Retrieval System (NPIRS) to determine which pesticides are registered in their state: http://npirspublic.ceris.purdue.edu/state/. An integrated pest and pollinator management approach requires growers to be aware of their pest populations through scouting early and often, to use non-chemical methods when effective, and when pesticides are warranted - to choose products that are effective and pose the lowest risk to bees and other non-target organisms. IPPM: Putting the “Pollinator” in IPM: 1) If spray is necessary, spray in the evening when pollinators are not foraging on the crop or nearby wildflowers 2) Read the entire product label to find pollinator protection guidelines during application, and follow label directions. 3) Select pesticides that are effective against target pests, but least toxic to bees. 4) Avoid using pesticides or tank mixing pesticides and adjuvants that are noted in this guide to synergize with each other. 5) Choose sprayer nozzles and settings that reduce drift. Follow label ©van Dyke directions regarding wind speed and temperature inversions to Bees visit flowers, like willow, in 1 avoid drift to areas of potential bee habitat at field edges. field edges when crop is not in 6) Unless the product label notes otherwise, avoid applying bloom1. insecticides when high humidity at low temperatures are forecasted following application. Dew is common under these conditions, which allows residues to remain toxic up to twice as long. 7) Prevent bees from visiting between crop rows while pesticides are being applied by mowing flowering weeds (e.g., dandelions) or mulching. Bees visiting these weeds can be exposeed to pesticides. 8) Follow label directions to reduce contamination of Keeping orchard rows free of flowering weeds surface waters (e.g., irrigation ditches, retention ponds, before pesticide applications minimizes bee creeks) where bees actively collect water and mud. exposure to pesticides. ©McArt 9) Develop a communication strategy to alert nearby beekeepers at least 24 hours in advance of applying a highly toxic pesticide. Consider using a written pollination contract with beekeepers who provide pollination services to discuss an IPPM plan in advance. An example template can be found in Appendix A of this guide.

6 Table 1. Product formulations and their active ingredients Product Name Active ingredient Product Name Active ingredient Product Name Active ingredient Fungicides including antibiotics Endura Boscalid Quali-Pro mef. mefenoxam Abamectin N-methyl-2-pyrrolidone Equus products chlorothalonil Quali-Pro myclo. myclobutanil (ingredient in) (NMP) Exilis plus N-methyl-2-pyrrolidone Quash metconazole Abound azoxystrobin Exponent piperonyl butoxide QuiltXcel azoxystrobin + propiconazole Academy difenoconazole + fludioxonil Ferbam Ferbam Quintec quinoxyfen Acadia azoxystrobin Fireline oxytetracycline Rally 40 WSP myclobutanil Actigard acibenzolar-s-methyl Firewall streptomycin Ranman 400SC cyazofamid Aframe azoxystrobin Flint trifloxystrobin Regalia reynoutria Aframe Plus azoxystrobin + propiconazole Flint Extra trifloxystrobin Rhyme flutriafol Agricure potassium bicarbonate FontelisNY penthiopyrad Ridomil Gold SL mefenoxam Agri-mycin streptomycin Fortix flutriafol Rovral 4F iprodione Aliette fosetyl-al Fortuna mancozeb Scala pyrimethanil AlsaNY propiconazole Fungisol debacarb Scholar fludioxonil Amistar Top azoxystrobin + Gem 500 SC trifloxystrobin Sercadis (Xemium) fluxapyroxad difenoconazole Glacial Spray mineral oil Serenade ASO§, Bacillus subtilis Aprovia benzovindiflupyr Heritage azoxystrobin Max§, and Opti§ AproviaTop benzovindiflupyr + Incognito 4.5F thiophanate-methyl Sonoma 40 WSP myclobutanil difenoconazole Indar2F fenbuconazole SovranNY† kresoxim-methyl Ardent N-methyl-2-pyrrolidone Initiate 720 & ZN chlorothalonil Streptrol streptomycin (ingredient in) (NMP) InspireSuper difenoconazole + cyprodinil SubdueGR mefenoxam- nonbearing Azoxystar azoxystrobin Iprodione2F Select iprodione Subtilex NG Bacillus subtilis Badge SC & X2§ copper oxychloride + copper Kaligreen potassium bicarbonate Sulfur sulfur hydroxide Kasumin 2L kasugamycin Syllit FL dodine Banner Maxx propiconazole Kestrel MexNY propiconazole Tartan trifloxystrobin Biocover MLT mineral oil Kocide HCu, 2000- copper hydroxide Temprano N-methyl-2-pyrrolidone Bonide complete captan O§ & 3000-O§ (ingredient in) (NMP) fruit tree spray Luna Sensation† fluopyram + trifloxystrobin Terraguard* triflumizole Bonide Fruit Tree boscalid + pyraclostrobin + Luna Tranquility† fluopyram + pyrimethanil Tilt propiconazole & Plant Guard lambda- ManKocide mancozeb + copper hydroxide Topguard† flutriafol Bravo chlorothalonil Manzate mancozeb Topguard EQ† azoxystrobin+flutriafol Bravo Ultrex chlorothalonil Flowable* Topsin M thiophanate-methyl BroadformNY† fluopyram Manzate Max T&O mancozeb Torino cyflufenamid Bromazil†† imazalil†† Manzate ProStick mancozeb Tourney metconazole Bumper ES propiconazole Marazo propiconazole Triathlon BA§ Bacillus amyloliquefaciens C-O-C-S WDG copper oxychloride + copper Mastercop copper sulfate Ultra Flourish mefenoxam sulfate Merivon (BASF)NY† fluxapyroxad + pyraclostrobin Vango ESQ difenoconazole + cyprodinil Cabrio EG pyraclostrobin Meteor iprodione Vango WG cyprodinil Camelot O§ copper octanoate MilStop potassium bicarbonate Vanguard WG cyprodinil Cannonball fludioxonil MoncoatMZ flutolanil + mancozeb Vault Bacillus amyloliquefaciens Captan 50 WP captan Monterey Bacillus amyloliquefaciens Velum PrimeNY† fluopyram Captan 80 WDG captan Complete§ Vivando metrafenone CaptEvate 68WDG fenhexamid + captan Mural benzovindiflupyr + Warden RTA mefenoxam + fludioxanil Catamaran chlorothalonil + potassium azoxystrobin WillowoodEPA abamectin phosphite MycoShield oxytetracycline Ziram Ziram Cease§ Bacillus subtilis Nevado iprodione Zoro N-methyl-2-pyrrolidone Champ§ copper hydroxide Omni 6E mineral oil (ingredient in) (NMP) Contans Coniothyrium minitans Oreon PCNB (quintozene or Products with mixtures of fungicides Crystalline BASF* pyraclostrobin pentachloronitrobenzene) products PBO-8 piperonyl butoxide and insecticides Cueva§ copper octanoate Penbotec 400 SC pyrimethanil Adage ST thiamethoxan + fludioxonil + Cuprofix Ultra 40 copper sulfate Penncozeb 75 DF mancozeb mefenoxam Cuproxat copper sulfate Phostrol phosphorous acid (salts) Bonide fruit tree & boscalid + pyraclostrobin + Curzate 60 DF cymoxanil Polyram 80 DF metiram plant guard lambda-cyhalothrin Decco Pyr. 400 SC pyrimethanil PresidioNY fluopicolide Cruiser Maxx thiamethoxan + fludioxonil + Deccozil†† imazalil†† Previsto copper hydroxide mefenoxam Decree 50 WDG fenhexamid Pristine boscalid + pyraclostrobin Ethos Bacillus amyloliquefaciens + Difenoconazole difenoconazole Procure* triflumizole NY Prophyt (Helena) phosphorous acid (potassium 3L Insecticides and insect growth Dithane mancozeb phosphite) Propi Max propiconazole regulators Double Nickel§ Bacillus amyloliquefaciens EPA Echo 90 DF & Lite chlorothalonil Pure Spray 10E, mineral oil Abamex abamectin EFOG-160-PYR pyrimethanil 15E, 22E AcetoEPA bifenthrin storage Quadris F azoxystrobin Acramite bifenazate Elevate 50 WDG fenhexamid Quadris Opti azoxystrobin + chlorothalonil Actara NY† thiamethoxam Empress Intrinsic Pyraclostrobin Quadris Top azoxystrobin + Admire ProNY imidacloprid Encartis boscalid + chlorothalonil difenoconazole Advise 4NY imidacloprid

7 Agree WG§ Bacillus thuringiensis FanfareEPA bifenthrin PyGanic§ AgriProduct-FlexEPA Name/NY† abamectin Active ingredient+ thiamethoxam FascinationProduct Name benzyladenine Active ingredient + gibberellins PyrenoneProduct Name pyrethrin Active ingredient Insecticides and insect growth FastacEPA alpha- Radiant SC spinetoram Flagship 25WGNY† thiamethoxam Regent†† fipronil†† (discontinued) regulators (continued) EPA/NY EPA Flonicamid 50WG flonicamid Return † Agri-Mek abamectin NY AltacorNY† Floramite bifenazate Rimon novaluron Ammo cypermethrin Fyfanon Safer§ insecticidal soap AnnihilateEPA/NY GameStop§ kaolin Savey hexythiazox Apistan tau-fluvalinate Gaucho 480 imidacloprid Seduce Insect spinosad Apollo clofentezine Gaucho 600 imidacloprid Bait§ Applaud IGRNY Gaucho XT imidacloprid Sepro Akari fenpyroximate Aquaflow tau-fluvalinate GibGro gibberellic acid Sevin GladiatorEPA zeta-cypermethrin + ShuttleO acequinocyl Arvida acetamiprid EPA/NY Asana XLEPA avermectin Silencer lambda-cyhalothrin Assail acetamiprid Gnatrol Bacillus thuringiensis SpinTor 2SC§ spinosad subspecies and proteins Spirotetramat spirotetramat Avaunt Indoxacarb HeroEPA bifenthrin + piperonyl 240SC Aza-Direct§ azadirachtin butoxide Steward indoxacarb AzaGuard azadirachtin ImidanNY SuffOil-X§ petroleum oil Azatin§ azadirachtin IntrepidNY† methoxyfenozide SultrusEPA beta- Azomar acetamiprid IntruderMax acetamiprid Sunspray petroleum oil Banter bifenazate EPA Javelin§ Bacillus thuringiensis Surround 95 WP§ kaolin Baythroid XL beta-cyfluthrin NY EPA subspecies and proteins Talus 70DF † buprofezin Baythroid cyfluthrin JMS Stylet§ horticultural oil TempoNY beta-Cyfluthrin Beleaf products flonicamid Kanemite acequinocyl Thuricide Bacillus thuringiensis Belt SC*† (discontinued) EPA/NY Kopa§ insecticidal soap subspecies and proteins Besiege † chlorantraniliprole + lambda- Lannate LVEPA & methomyl Timectin 0.15EC abamectin cyhalothrin EPA EPA SP AG Bifenture bifenthrin Leverage 360EPA beta-cyfluthrin + TombstoneEPA cyfluthrin BioBit Bacillus thuringiensis imidacloprid Tourismo*† flubendiamide (discontinued) subspecies and proteins Lorsban 4EEPA & Triact 70§ extract of neem oil Bonideoil§ horticultural oil AdvancedEPA Trilogy§ extract of neem oil Brigade bifenthrin EPA EPA EPA M1-LV methomyl Tundra bifenthrin 10WSB † NY NY EPA Macho 2 & 4 imidacloprid Ultra-Fine horticultural oil Brigade 2EC bifenthrin Magister fenazaquin VendexEPA fenbutatin-oxide Calypso 4 thiacloprid Magus fenazaquin VentasEPA/NY† oxamyl Flowable†† Mavrik tau-fluvalinate VerveNY ethephon Carbaryl 4L carbaryl Molt-X azadirachtin Voliam FlexiNY† thiamethoxam + CentaurNY† buprofezin NY Monterey B.T.§ Bacillus thuringiensis chlorantraniliprole Collate ethephon EPA NY subspecies and proteins Warrior II Zeon lambda-cyhalothrin Confirm † Movento spirotetramat Xentari Bacillus thuringiensis Cruiser 5SC thiamethoxam M-pede§ insecticidal soap subspecies and proteins Damoil horticultural oil EPA EPA/NY Mustang & piperonyl butoxide & zeta- Zeal etoxazole Danitol Mustang MAXXEPA cypermethrin ZetaGuard LBT zeta-cypermethrin + PBO Delegate WG spinetoram Nealta cyflumetofen Adjuvants, stickers, inert ingredients, Demand SC, EZ & lambda-cyhalothrin Neemix§ azadirachtin G and registered synergists Nexter† pyridaben Activator90 polyethoxylated nonylphenol Des-X§ insecticidal soap N-Large gibberellic acid EPA (N-90) AG500 diazinon Novagib gibberellic acid EPA Butacide piperonyl butoxide Diazinon 50W diazinon NudrinEPA/NY methomyl NY Crossfire polyethoxylated nonylphenol dimethoate Omni acetamiprid EPA (N-90) Dimilin Onager hexythiazox DiPel DF Bacillus thuringiensis Induce non-ionic surfactant Pedestal novaluron LI-700 non-ionic surfactant subspecies and proteins Perimeter tau-fluvalinate Drexel carbaryl carbaryl MustangEPA & piperonyl butoxide & zeta- NY Phase organosilicone surfactant EPA Durivo † thiamethoxam + NY Mustang MAXX cypermethrin Platinum 75 SG † thiamethoxam N-90 polyethoxylated nonylphenol chlorantraniliprole Portal fenpyroximate EPA (N-90) Endigo ZC † thiamethoxam + lambda- Pounce 25 WPEPA EPA/NY Phase organosilicone surfactant Endigo ZCX † cyhalothrin ProclaimEPA/NY emamectin benzoate Entrust SC§ spinosad Pybuthrin piperonyl butoxide NY ProGibb 4% gibberellic acid Envidor † spirodiclofen NY Regulaid non-ionic surfactant Provoke imidacloprid Silicone organosilicone surfactant Esteem Pure Spray§ horticultural oil NY Silkin organosilicone surfactant Exirel † (Dupont) Pycana pyrethrin Falgro gibberellic acid Silt organosilicone surfactant

8 Table 2. Pesticide synergies and acute, chronic, and sublethal toxicities for honey bees and other pollinators Key to table abbreviation, symbols, and colors EPA - EPA Federally Restricted-Use Pesticide product NY - New York State Restricted-use pesticide in New York Restricted-Use Pesticide product - Not for use in Nassau and Suffolk counties (Long Island) of New York - Not for use in New York state on apple - Meets USDA organic standards - Identifies a chemical that at least one study has shown synergy with other active ingredients or products. - Identifies a formulation containing more than one active ingredient, at least one of which has been shown to synergize with other chemicals EPA standard toxicity ratings: acute oral and/or contact toxicity to the honey bee (Apis mellifera)

- Highly toxic (acute LD50 < 2μg/bee)

- Moderately toxic (acute LD50 2 - 10.99μg/bee)

- Practically non-toxic (acute LD50 >11 μg/bee)

Fungicides including antibiotics Active Ingredient New York High Moderate Practically Synergies, sublethal effects, and toxicity to bee Chemical group Trade Name toxicity toxicity non-toxic species other than the honey bee [Resistance code] Examples acibenzolar-S-methyl Actigard benzothiadiazole [P01] azoxystrobin Quadris F, The combination of Quadris® (azoxystrobin) and 2SE QoI-methoxy-acrylate Abound, Select® (iprodione) produce a low level synergy (still fungicide [11] Acadia, practically non-toxic) in late season honey bees that Aframe, increases with time from application; 60% mortality at Heritage 10 days2. No synergy detected with thiacloprid3. azoxystrobin + Amistar Top, See azoxystrobin and difenoconazole separately for difenoconazole Quadris Top synergy information. QoI-methoxy-acrylate + DMI-triazole fungicide [11+3] azoxystrobin + flutriafol Topguard EQ† QoI-methoxy-acrylate + DMI-triazole fungicide [11+3]

azoxystrobin + Aframe Plus, See azoxystrobin and propiconazole separately for propiconazole Quilt Xcel synergy information. QoI-methoxy-acrylate + DMI-triazole fungicides [11+3]

9 Active Ingredient New York High Moderate Practically Synergies, sublethal effects, and toxicity to bee Chemical group Trade Name toxicity toxicity non-toxic species other than the honey bee [Resistance code] Examples Bacillus amyloliquefaciens Double Microbial disruptor of Nickel§, pathogen produced by natural Monterey Complete§, bacterium [44] Triathlon BA§, Vault IP Bacillus subtilis Cease§, The wet application of B. subtilis strain QST713 Microbial disruptor of Serenade (Serenade®) reduced honey bee brood production and pathogen, toxin produced by (ASO, Max, was highly toxic to the bumble bee (Bombus terrestris)4. and Opti,)§, natural bacterium [44] Tests on the dry application of B. subtilis strain QST713 Subtilex NG (Serenade®) and strain QRD132 (Serenade®) did not significantly impact Bombus impatiens5 or honey bees6. benzovindiflupyr AproviaNY, A new product for bitterrot. NY SDHI-pyrazole-4-carboxamide Elatus fungicide [7] boscalid Endura Synergizes with clothianidin and thiamethoxam7. SDHI-pyridine-carboxamide (grape; co- fungicide [7] occuring crop) boscalid + pyraclostrobin , Pristine® (boscalid+pyraclostrobin) synergizes with SDHI-pyridine-carboxamide + Pristine chlorpyrifos8 reducing queen emergence due to QoI- methoxy-carboxamide compromised immunity. Pristine® synergizes with fungicides [7+11] Iprodione 2SE Select® (iprodione) increasing honey bee mortality2, and with Rovral® (iprodione) negatively impacting solitary bee species nesting behavior9. Shows no synergy with chlorantraniliprole, methoxyfenozide or diflubenzuron10. captan Captan 50 Studies have found captan to increase honey bee brood phthalimide fungicide [M4] WP, Captan, mortality to a moderately toxic level11,12 and alter larval 80 WDG feeding capacity13. A study conducted by the USDA Bee Lab in Weslaco, TX found that the inert ingredients mixed with captan make it highly toxic14. Other laboratory studies report captan to be highly toxic to mason bees15 and leafcutter bees 16,17 but practically non-toxic to bumble bees at recommended field rates18. chlorothalonil Bravo ZN, Synergizes with alpha-cypermethrin increasing risk chloronitrile fungicide [M5] Bravo Ultrex, (toxicity x exposure) 10-fold19 and the beekeeping Echo miticide tau-fluvalinate 5-fold to moderate toxicity20. agricultural showed mixed results with a 5-fold decrease products, in honey bee larval survival in one study and only a Equus, Initiate 21 720 & ZN marginal decrease in adult survival in another study . Increased toxicity occurs when mixed with thymol20, but the toxicity is still below concern. Also synergizes with Cerconil® (thiophanate-methyl) exhibiting cumulative high oral toxicity in honey bee larvae reared on field relevant doses for 6 days21 and increases honey bee and bumble bee susceptibility to Nosema infection22,23 and entombed pollen inside the honey bee hive22.

10 Active Ingredient New York High Moderate Practically Synergies, sublethal effects, and toxicity to bee Chemical group Trade Name toxicity toxicity non-toxic species other than the honey bee [Resistance code] Examples copper hydroxide Kocide HCu, inorganic 2000-O§ & fungicide/bacteriacide [M1] 3000-O§, Champ§, Previsto copper octanoate Camelot O§, inorganic Cueva§ fungicide/bacteriacide [M1] copper oxychloride/ Badge SC & Copper oxychloride synergizes with imidacloprid24. copper hydroxide X2§ inorganic fungicide/bacteriacide [M1] copper oxychloride/copper C-O-C-S WDG Copper oxychloride synergizes with imidacloprid24. sulfate inorganic fungicide/bacteriacide [M1] copper sulfate Cuprofix Highly toxic to a stingless bee species via oral exposure25. inorganic Ultra, fungicide/bacteriacide [M1] Cuproxat, Mastercop cyflufenamid Torino cyprodinil Vanguard WG, Moderate toxicity when it synergizes with thiacloprid3. anilino-pyrimidine fungicide, Vango WG [9] difenoconazole Difenoconazole Synergizes with deltamethrin26 and the tau-fluvalinate27 NY DMI-triazole fungicide [3] 3L product Mavrik® inducing hypothermia in honey bees. In B. impatiens bifenthrin had a low synergy with difenoconazole, at 48 h and 72 h, 1.48-fold and 1.37-fold mortality, respectively but no synergy was detected with thiamethoxam28. difenoconazole + Academy See difenoconazole and fludioxonil separately for fludioxonil synergy information. DMI-triazole + phenylpyrroles fungicides [3+12] difenoconazole + cyprodinil Inspire Super, See difenoconazole and cyprodinil separately for synergy DMI-triazole + anilino- Vango ESQ information. pyrimidine fungicides [3+9] dodine Syllit FL guanidine fungicide [U12] fenbuconazole Indar 2F Synergizes with tau-fluvalinate20 making it highly toxic to DMI-triazole fungicide [3] honey bees. At a field relevant dose Indar 2F® (fenbuconazole) synergizes with acetamiprid29 in a solitary bee, doubling the toxicity of acetamiprid, making

it borderline highly toxic (LD50 2.1).

11 Active Ingredient New York High Moderate Practically Synergies, sublethal effects, and toxicity to bee Chemical group Trade Name toxicity toxicity non-toxic species other than the honey bee [Resistance code] Examples fenhexamid Decree 50 Fenhexamid, when tested, was found to have no synergy SBI-KRI hydroxyanilide WDG, Elevate with bifenthrin nor thiamethoxam28. fungicide [17] 50 WDG fenhexamid + captan CaptEvate 68 See captan separately for toxicity notes. SBI-KRI hydroxyanilides + WDG phthalimide [17+M4] ferbam Ferbam dithiocarbamate fungicide granuflo [M3] fludioxonil Cannonball, Impacts honey bee learning behavior30. phenylpyrroles fungicide [12] Scholar fluopicolide PresidioNY Used on landscape fruit trees only acylpicolide fungicide [U] fluopyram Velum NY pyridinyl-ethyl-benzamide Prime †, NY fungicide [7] Broadform † fluopyram + pyrimethanil Luna NY pyridinyl-ethyl-benzamide + Tranquility † anilino-pyrimidine fungicides [7+9] flutriafol Rhyme† Synergizes with lambda-cyhalothrin31,32 making lambda- DMI-triazole fungicide [3] cyhalothrin 3 times more toxic to honey bees (?). Although EPA classifies this pesticide as low toxicity to honey bees, the European Food Safety Authority determined it exhibits moderate toxicity when the a.i. is consumed by bees33 fluxapyroxad Sercadis NY† SDHI-pyrazole-4-carboxamide fungicide [7] fluxapyroxad + Merivon See pyraclostrobin separately for synergy information. NY pyraclostrobin Xemium † SDHI-pyrazole-4-carboxamide + methoxy-carboxamide fungicides [7+11] fosetyl-Al Aliette WDG aluminum tris (O- ethylphosphonate) fungicide [P07(33)] imazalil†† No products Synergizes with cypermethrin, fipronil, and DMI-imidazole fungicide [3] registered in thiamethoxam in bumble bees34 and lambda-cyhalothrin NY in honey bees32.

12 Active Ingredient New York High Moderate Practically Synergies, sublethal effects, and toxicity to bee Chemical group Trade Name toxicity toxicity non-toxic species other than the honey bee [Resistance code] Examples iprodione Meteor, Synergizes with Pristine® (pyraclostrobin+ boscalid)9. dicarboxamide fungicide [2] 26GT, Compass SC® (iprodione + thiophanate methyl), the Nevado, varroacide, Mavrik® (tau-fluvalinate)35 and decreases Rovral 4 F, the repellency of honey bees to cypermethrin19 thereby Iprodione 2F increasing their exposure. The combination of Iprodione Select 2SE Select® and Quadris® (azoxystrobin) is initially a low level synergy in late season honey bees that increases to 60% mortality 10 days after application2 . Iprodione mixed with a field relevant dose of chlorantraniliprole increases honey bee larval mortality 20-30%. No synergy with methoxyfenozide or diflubenzuron10. One study reports high toxicity to honey bee larvae12 and another reports sublethal effects on some solitary bees9. kasugamycin Kasumin 2L antibiotic [24] kresoxim-methyl SovranNY† QoI-oximino-acetate fungicide [11] mandipropamid + Revus Top See difenoconazole separately for synergy information. difenoconazole CAA mandelic acid amides + DMI- triazole fungicides [40+3] mancozeb DithaneNY, When combined with alpha-cypermethrin or lambda- NY dithiocarbamate fungicide Koverall , cyhalothrin studies found a 2-4 fold decrease in the [M3] Manzate, contact toxicities19 of these two insecticides on honey Penncozeb bees likely due to increased repellency. Synergy on 75DF honey bees not detected with thiacloprid3. mancozeb + copper ManKocideNY See mancozeb separately for synergy information. hydroxide dithiocarbamate fungicide + inorganic fungicide/ bactericide [M3+M1] mefenoxam (metalaxyl-M) Quali-Pro When mixed with thiamethoxam, mefenoxam reduces phenylamide acylalanine Mefenoxam, honey bee toxicity of the thiamethoxam36. [4] Ridomil Gold SL, Ultra Flourish metconazole Quash, Synergy with tau-fluvalinate20 causing a 3-4 fold increase DMI- triazole[3] Tourney in contact toxicity of this miticide. metiram Polyram 80DF dithiocarbamate fungicide [M3] metrafenone Vivando benzophenone fungicide [50]

13 Active Ingredient New York High Moderate Practically Synergies, sublethal effects, and toxicity to bee Chemical group Trade Name toxicity toxicity non-toxic species other than the honey bee [Resistance code] Examples myclobutanil Quali-Pro Synergizes with clothianidin, imidacloprid, DMI-triazole fungicide [3] myclobutanil, thiamethoxam37, lambda-cyahalothrin32,38, tau- Rally 40 WSP, fluvalinate20 via oral and/or contact exposure in honey Sonoma 40 bees. Synergy with lambda-cyhalothrin also affects WSP bumble bees feeding on pollen38. In B. impatiens thiamethoxam was found to synergize with myclobutanil 2.38-fold and bifenthrin was also found to synergize with myclobutanil increasing mortalityl at three time steps (24h, 48h, and 72h), by 2.56 3.28, and 11.0-fold, respectively28. Synergy is not detected with thiacloprid37. mineral oil Biocover MLT, Horticultural Spray Glacial Spray, Omni 6E, PureSpray 10E, 15E, & 22E oxytetracycline Fireline, One study found a synergy with tau-fluvalinate39 while tetracycline antibiotic MycoShield another study did not show synergy with tau- fluvalinate20. penthiopyrad Fontelis Low toxicity to adult honey bees but only found in larval NY pyrazole-4-carboxamide (Dupont) provisions40. fungicide [7] phosphorous acid Phostrol, sodium, potassium, and Helena ammonium salts of Prophyt phosphorus acid potassium bicarbonate Agricure, Inorganic salt Kaligreen, MilStop potassium phosphite Helena Inorganic salt Prophyt propiconazole AlsaNY, Propi Synergizes with alpha-cypermethrin32, acetamiprid, DMI-triazole fungicide [3] Max EC, imidacloprid, thiacloprid41,37, lambda-cyhalothrin32,19, Bumper ES tau-fluvalinate20, thiamethoxam37 and clothianidin in (non-bearing), honey bees. One study determined that propiconazole Kestrel MexNY, reduced the toxicity of thiacloprid37 to honey bees. Also Marazo, Tilt, Banner Maxx synergizes with clothianidin in bumble bees and some 42 II solitary bees however another study demonstrated only additive effects of clothianidin43. Propiconazole alone decreases bumble bee reproduction44. pyraclostrobin BASF Synergizes with fenpyroximate and the beekeeping QoI-methoxy-carboxamide Crystalline miticide tau-fluvalinate20. The product mixture Pristine® fungicide [11] products, (pyraclostrobin + boscalid) synergizes with 2SE Select® Cabrio EG, (Iprodione)2 and negatively impacts foraging and nesting Empress success of some solitary bees9 and immunity in honey Intrinsic bees8. When combined with fipronil††, honey bee larval feeding decreases45.

14 Active Ingredient New York High Moderate Practically Synergies, sublethal effects, and toxicity to bee Chemical group Trade Name toxicity toxicity non-toxic species other than the honey bee [Resistance code] Examples pyrimethanil Decco Pyr. anilino-pyrimidine fungicide 400 SC, Scala, [9] Penbotec 400 SC, EFOG-160 quinoxyfen Quintec azanaphthalene aryloxyquinoline fungicide [13] reynoutria Regalia Botanical extract of Biofungicide Reynoutria sacchalinensis streptomycin Agri-mycin, antibiotic [25] Streptrol, Firewall sulfur Sulfur, Some Moderate oral toxicity can remain up to 7 days46. inorganic natural element products § [M2] thiophanate-methyl Topsin M Synergizes with tau-fluvalinate19,20, , and thiophanate fungicide [1] products, lambda-cyhalothrin19 becoming highly toxic to honey Incognito 4.5F bees. Synergizes with product formulations containing the active ingredients imidacloprid, or chlorothalonil47 to become highly toxic to honey bees and other bees when consumed. trifloxystrobin Flint, Flint methoxy-carboxamide Extra, Gem fungicide [11] 500SC triflumizole ProcureNY, Synergizes with acetamiprid, imidacloprid, and TerraguardNY 41 imidazole fungicide [3] thiacloprid . ziram Ziram dithio- fungicide [M3] Mixtures of fungicides and insecticides Active Ingredient New York High Moderate Practically Synergies, sublethal effects, and toxicity to bee Chemical group Trade Name toxicity toxicity non-toxic species other than the honey bee [Resistance code] Examples Bacilluls amyloliquefaciens Ethos 3DEPA See bifenthrin for toxicity and synergy information. + bifenthrin Microbial disruptor of pathogen produced by natural bacterium + insecticide [44+3A]

15 Active Ingredient New York High Moderate Practically Synergies, sublethal effects, and toxicity to bee Chemical group Trade Name toxicity toxicity non-toxic species other than the honey bee [Resistance code] Examples thiamethoxam + Adage ST, See thiamethoxam, fludioxonil, and mefenoxam fludioxonil + mefenoxam Cruiser MAXX separately for synergy and toxicity information nitro- insecticide + phenyl pyrrole + phenyl amide acylalanine fungicides (4A+12+ 4) Insecticides including insect growth regulators Active Ingredient New York High Moderate Practically Synergies, sublethal effects, and toxicity to bee Chemical group Trade Name toxicity toxicity non-toxic species other than the honey bee [Resistance code] Examples abamectin /avermectin Agri -MekEPA, Vertimec® (abamectin) formulation which includes avermectin insecticide [6] AbamexEPA, unknown inert ingredients produces a synergistic Timectin 0.15 response that was 709x /1870x more toxic to honey EC AGEPA, bees and Melipona bees than the active ingredient, Willowood abamectin alone48. Highly toxic both topically and orally 0.15LVEPA to honey bees49 and arrests reproduction in bumble bees50. Other non-honey bee species exhibits moderate to high toxicity via contact and oral exposure, 51 respectively . abamectin + Agri- See abamectin separately for toxicity information and thiamethoxam FlexEPA/NY† thiamethoxam separately for synergy information. avermectin + nitro- neonicotinoid insecticide [6+4A] acequinocyl Kanemite, Topical and oral exposure arrests bumble bee 50 quinolone insecticide [20B] Shuttle O reproduction . acetamiprid Assail 30 SG, Synergizes with piperonyl butoxide (PBO), S,S,S- cyano-neonicotinoid Arvida 30 SG, tributylphosphorotrithioate (DEF), triflumizole41, insecticide [4A] Azomar, propiconazole41,38, and Indar2® (fenbuconazole)29 Omni- making these highly toxic mixtures. Synergy with acetamiprid, propiconazole38 and Indar2® (fenbuconazole)29 is also Intruder Max present in bumble bees and mason bees respectively. One study shows 3-fold of Bombus impatiens to Assail® (acetamiprid) alone and 1.5-fold toxicity to the combination of Assail® and Tilt® (propiconazole) by decreasing honey bee worker body size. alpha-cypermethrin FastacEPA Synergizes with imazalil in at least one bumble bee pyrethroid insecticide [3A] species34. In honey bees, Alpha-cypermethrin, an isomer of cypermethrin, synergizes with Bravo SC® (chlorothalonil), Tilt EC® (propiconazole), and Sportak EW® (prochloraz), and increases toxicity of Derosal WG® 80% (carbendazim), Compass SC® 15.5%/15.5% (iprodione + thiophanate methyl) and other triazoles including Folicur EW® (tebuconazole) and Plover EC® (difenoconazole)19. Both cypermethrin and zeta-cypermethrin are highly toxic to solitary bees52. Cypermethrin increases Chronic Paralysis 53 Virus (CPV) infection .

16 Active Ingredient New York High Moderate Practically Synergies, sublethal effects, and toxicity to bee Chemical group Trade Name toxicity toxicity non-toxic species other than the honey bee [Resistance code] Examples azadirachtin Aza-Direct§, Oral exposure below, at, and above a field relevant dose Naturally occurring AzaGuard, causes bumble bee worker mortality and sublethal tetranortriterpenoid Molt-X, effects on reproduction and body mass54. Insect growth regulator [UN] Neemix§, Azatin§ Bacillus thuringiensis AgreeWG§, Negative sublethal impacts on honey bee physiology55. subspecies and proteins BioBit, DiPel Microbial disruptor of DF, Gnatrol, insect midgut Javelin WG§, membranes [11A] Monterey B.T.§, Thuricide, Xentari beta-Cyfluthrin Baythroid The parent chemical, cyfluthrin synergizes with piperonyl pyrethroid insecticide [3A] XLEPA, butoxide56 becoming 30 times more toxic to honey bees. SultrusEPA, It also impacts honey bee behavior56 and is highly toxic NY 38,57 Tempo SC topically and orally to bumble bees beta-Cyfluthrin + Leverage See cyfluthrin and imidacloprid separately for synergy imidacloprid 360EPA and toxicity information. pyrethroid + cyano- neonicotinoid insecticide [3A+4A] bifenazate Acramite-4SC, Moderate and High toxicity, topically and orally, Insect growth regulator [20D] Banter-4SC, relatively to bumble bees including sublethal effects at 1 1 50 Floramite SC just /10 - /2 MFRC . Honey bee mortality increased 5- fold, 10 days after exposure58. bifenthrin AcetoEPA, Synergizes with the miticide Apistan® (tau-fluvalinate)59. pyrethroid insecticide [3A] BifentureEPA, Highly toxic to bumble bees59,38 however bifenthrin Brigade residue is typically not frequently found in pollen and WSBEPA†, nectar38. Pyrethroids in general are well known to Brigade ECEPA, synergize with piperonyl butoxide and triazole FanfareEPA, fungicides19,32,60–62. In B. impatiens, bifenthrin was also EPA Tundra EC found to synergize with myclobutanil increasing mortalityl at three time steps (24h, 48h, and 72h), by 2.56 3.28, and 11.0-fold, respectively and bifenthrin to have a low synergy with difenoconazole at 48 h and 72 h, of 1.48-fold and 1.37-fold mortality increase, respectively28. bifenthrin + zeta- HeroEPA See bifenthrin, zeta-cypermethrin and piperonyl cypermethrin w/ piperonyl butoxide separately for other synergy information. butoxide Piperonyl butoxide is a well known synergist with pyrethroid insecticide + pyrethroids like bifenthrin. Highly toxic to bumble bees59,38. synergist [3A+synergist] buprofezin Applaud The product formulation Buprofezin 65% WP® exhibits Insect growth regulator [16] IGRNY†, moderate toxicity48. Centaur WDGNY†, Talus 70DFNY†

17 Active Ingredient New York High Moderate Practically Synergies, sublethal effects, and toxicity to bee Chemical group Trade Name toxicity toxicity non-toxic species other than the honey bee [Resistance code] Examples carbaryl Sevin Highly toxic to bee species other than the honey bee63. carbamate insecticide [1A] Carbaryl, Used as a thinner at petal fall it impacts the bee Drexel community that typically are still visiting petal-less Carbaryl, flowers. Carbaryl 4L chlorantraniliprole AltacorNY† One study showed that field relevant doses of the a.i.’s anthranilic diamide insecticide chlorantraniliprole and propiconazole synergize, [28] reducing larval survival to adulthood 7.2 fold and that combining chrlorantraniliprole with iprodione increased larval mortality about 30%10. However, another study showed no detected synergy with propiconazole in honey bees64. Suppresses reproduction in worker bumble bees65. chlorantraniliprole + BesiegeEPA/NY† See chlorantraniliprole and lambda-cyhalothrin lambda-cyhalothrin separately for synergy and toxicity information. anthranilic diamide + pyrethroid insecticide [28+3A] chlorpyrifos Lorsban-4EEPA, Synergizes in honey bees with propiconazole66 doubling organophosphate insecticide Lorsban the toxicity; with cypermethrin67 exponentially [1B] AdvancedEPA increasing toxicity overtime 15-fold at 7 days. When combined with the product formulation Pristine® (pyraclostrobin + boscalid) it reduces honey bee queen emergence8. Highly toxic to bumble bees68,69,38, solitary 51 21 bees and chronically lethal to honey bee larvae . chlorpyrifos + bifenthrin Tundra See bifenthrin and chlorpyrifos separately for synergy organophosphate + pyrethroid SupremeEPA and toxicity information. insecticide [1B+3A] clofentezine Apollo tetrazine ovicide/miticide, an insect growth inhibitor [10A] cyantraniliprole Dupont If applied during flowering, cyantraniliprole causes anthranilic diamide insecticide ExirelNY† negative effects on honey bee survival, flight activity and [28] behavior as well as negative effects on bumble bee queen survival70. cyflumetofen Nealta beta-ketonitrile miticide [25A] cyfluthrin TombstoneEPA Synergizes with piperonyl butoxide56 becoming 30 times pyrethroid insecticide [3A] more toxic to honey bees. It also impacts honey bee behavior56 and is highly toxic topically and orally to bumble bees38,57 diazinon Diazinon Highly toxic to bumble bees and some solitary bees as organophosphate insecticide 50WEPA, well as honey bees71,63. [1B] Diazinon AG500EPA diflubenzuron DimilinEPA Reduces honey bee larval survival by 77.5%-100%10. Insect growth regulator [7C] Sublethal effects have also been shown on larvae and of 72–77 78 adult honey bee fertility ; but see .

18 Active Ingredient New York High Moderate Practically Synergies, sublethal effects, and toxicity to bee Chemical group Trade Name toxicity toxicity non-toxic species other than the honey bee [Resistance code] Examples dimethoate Drexel Highly toxic to bumble bees and some solitary bees 79,15. organophosphate insecticide DimethoateNY [1B] emamectin benzoate ProclaimEPA/NY avermectin insecticide [6] esfenvalerate Asana XLEPA Highly toxic to bumble bees51,38 and exhibits sublethal pyrethroid insecticide [3A] effects on megachilid bees80. ethephon CollateNY, insect growth regulator VerveNY etoxazole Zeal Highly toxic to bumble bees when consumed50,55. etoxazole insecticide [10B] fenazaquin Magister, Low toxicity to bumble bees57 pyridazine insecticide [21A] Magus fenbutatin-oxide Vendex EPA organotin insecticide [12B] 50WP †† (EXPIRED) Reduces reproduction and the size of winter honey bee 76 Insect growth regulator [7B] colonies . fenpropathrin Danitol Highly toxic to bumble bees and some solitary bees81. EPA/NY pyrethroid insecticide [3A] 2.4 fenpyroximate Portal, Sepro Synergizes with enzyme inhibitors piperonyl butoxide pyridazine insecticide [21A] Akari (PBO) and S,S,S-tributylphosphorotrithioate (DEF), fungicides including prochloraz, pyraclostrobin and beekeeping miticides amitraz20, and oxalic acid making these mixes highly toxic. And in the cases of the beekeeping miticides tau-fluvalinate and coumaphos20 borderline high toxicity (LD50 2.04-2.4). Although EPA has reported that this active ingredient is practically non- toxic, one study measured moderate toxicity to honey bees20. fipronil†† Regent Synergizes with imazalil to be lethal to bumble bees at phenyl pyrazole fungicide [2B] discontinued 24 hrs but the toxicity subsides by 48 hrs34. Fipronil†† is associated with increased Nosema infection82. flonicamid Beleaf 50SG, flonicamid insecticide [29] Flonicamid 50WG flubendiamide†† Belt SC*† Moderate toxicity when applied topically to honey bees anthranilic diamide insecticide discontinued, has been reported in laboratory and semi-field [28] Tourismo*† conditions83. Megachile rotundata84 and Bombus discontinued impatiens85 were not impacted by Belt SC® (flubendiamide). gibberellic acid Falgro, Also used as a supplement in the honey bee diet86. Insect growth regulator Novagib, GibGro, N- Large, Pro- Gibb 4%§

19 Active Ingredient New York High Moderate Practically Synergies, sublethal effects, and toxicity to bee Chemical group Trade Name toxicity toxicity non-toxic species other than the honey bee [Resistance code] Examples hexythiazox Hexygon, thiazolidine insecticide [10A] Savey, Onager horticultural oil Bonide Products with thymol, menthol, and rosemary can be mineral oil horticultural highly toxic, especially when bees are already stressed87– oil§, Damoil, 90). Bees are temporarily inactivated by direct contact JMS Stylet§, with oil sprays; death may occur91. PureSpray§, Sunspray Ultra-Fine horticultural oil Suffoil-X, Bees show temporary inactivity by direct contact with oil petroleum oil Sunspray 6E sprays; death may occur91. imidacloprid Advise 4NY, Synergizes with piperonyl butoxide41,92, propiconazole41, nitro-neonicotinoid insecticide Admire Pro triflumizole41, Advise 2FL® (imidacloprid) synergized with [4A] Systemic Vydate 3.77 CLV® (oxamyl), Transform 5G® (sulfloxaflor), ProtectantNY, and Domark ME® (tetraconazole)92. Highly toxic to Macho 2NY & bumble bees93. May impact groundnesting bees94. 4NY, ProvokeNY indoxacarb Avaunt High toxicity even at field-realistic doses83,95. oxadiazine insecticide [22A] insecticidal Soap M-pede§, The product Safer #567, not listed here, contains Repellant Des-X§, that are harmful to bees if they come into Kopa§, Safer§ direct contact during spraying. kaolin Surround Repellant WP§ lambda-cyhalothrin Demand CSNY Synergizes with flutriafol31, imazalil, myclobutanil, pyrethroid insecticide [3A] DUONY & EZNY, propiconazole32, prochloraz31,32,61, and piperonyl SilencerEPA, butoxide (16x increase)31,56. While a combination with Warrior II w/ mancozeb decreased toxicity 2-4 fold19. Highly toxic to ZeonEPA bumble bees81 and some solitary bees81,96. malathion Fyfanon Highly toxic to bumble bees and some solitary bees97 organosphosphate insecticide especially during daytime application98. [1B] Supracide Realistic field exposure moderately toxic38. organosphosphate insecticide [1B] methomyl AnnihilateEPA/ Moderately to Highly toxic to bumble bees99,57. carbamate insecticide [1A] NY, Dupont Lannate SPEPA & Lannate LVEPA, M1- LVEPA, Nudrin LVEPA/NY methoxyfenozide IntrepidNY† Acute and chronic effects to honey bee larvae and adults diacylhydrazine insecticide over time58. [18] insect growth regulator

20 Active Ingredient New York High Moderate Practically Synergies, sublethal effects, and toxicity to bee Chemical group Trade Name toxicity toxicity non-toxic species other than the honey bee [Resistance code] Examples Neem Triact 70§, Oral exposure at field relevant dose causes honey bee Trilogy XL larval mortality and sublethal effects on adult body size100–102. non-ionic surfactant Regulaid, LI-700, Induce novaluron Pedestal, Sublethal impacts on egg and larvae of honey bees103, insecticide [15] RimonNY some bumble bees94,104 and leafcutter bees94,105. oxamyl ReturnEPA/NY†, DuPont Vydate 3.7CLV® (oxamyl) synergizes with carbamate insecticide [1A] VentasEPA†, Advise2FL®(imidacloprid)92. No documented effects on Dupont bumble bees55. Vydate 2LEPA† permethrin Pounce 25 Synergizes with piperonyl butoxide106. Highly toxic to pyrethroid insecticide [3A] WPEPA, bumble bees81,107 and solitary bees81,108. Pounce 1.5GEPA phosmet ImidanNY Highly toxic to some solitary bees81. There are often high organophosphate insecticide residues in pollen samples38. [1B] pyrethrin PyGanic crop Synthetic forms synergize with multiple pesticide pyrethrin insecticide [3A] protection§, ingredients. See pyrethroids. Some formulations found 109 Pycana, to decrease honey bee body temperature . Pyrenone pyridaben Nexter† pyridazine insecticide [21A] pyriproxyfen Esteem Exhibits sublethal impacts on honey bee larvae, adult Insect growth regulator [7C] behavior, and survival58,110 as well as bumble bee larvae111. spinetoram Delegate WG, Oral exposure caused lethal and sublethal effects on spynosin insecticide [5] Radiant SC reproduction on Bombus terrestris112. Radiant SC® was found to be highly toxic topically but only mildly toxic orally to honey bees113. spinosad Entrust SC§, Moderate contact and high oral acute toxicity to bumble spynosin insecticide [5] Seduce§, bees114,94,112 as well as sublethal foraging effects115 on SpinTor 2SC§ bumble bees. One non-Apis bee species experienced moderate contact toxicity94 while three other species experienced high contact toxicity94,116,25 with one of those experiencing impaired flight116. spirodiclofen EnvidorNY† Although EPA classifies spirodiclofen as low toxicity, one tetronic acid insecticide [23] study finds moderate toxicity to adult honey bees117. Chronic exposure significantly reduced honey bee118 and 50 bumble bee reproduction and colony strength . spirotetramat Movento, Moderate acute toxicity and high chronic oral toxicity tetramic acid insecticide [23] Spirotetramat and sublethal reproductive effects to bumble bees119,5. 240 SC Moderately toxic to honey bee larvae in laboratory 120 studies with doses above field recommendations .

21 Active Ingredient New York High Moderate Practically Synergies, sublethal effects, and toxicity to bee Chemical group Trade Name toxicity toxicity non-toxic species other than the honey bee [Resistance code] Examples tau-fluvalinate (beekeeping) Apistan, Synergizes with boscalid20, chlorothalonil21,20, pyrethroid insecticide [3A] Aquaflow, fenbuconazole, metconazole, myclobutanil, prochloraz, a beekeeping miticide. Perimeter, propiconazole20, piperonyl butoxide56,20 as well as Mavrik beekeeping miticides coumaphos60,20, thymol, amitraz, fenpyroximate, and oxalic acid20. Highly toxic to honey bee larvae21. One study on Mavrik® (tau-fluvalinate) and the product ERIA® (difenoconazole+ carbendazim) resulted in no lethal or sublethal effects on bees27. tebufenozide ConfirmNY† Exhibits sublethal effects on honey bee behavior and 75,72 Insect growth regulator [7c] learning .

3 41 thiacloprid *This product is Calypso 4 Synergizes with cyprodinil , piperonyl butoxide , suspended, please dispose. Flowable†† triflumizole and propiconazole39,noted in 29 and is cyano-neonicotinoid associated with increased Nosema infection in honey insecticide [4A] bees82. However, one study found no synergy when mixed with tebuconazole, propiconazole or myclobutanil37. Field relevant exposure is lethal to 121 bumble bee colonies . thiamethoxam ActaraNY†, Synergizes with boscalid7, propiconazole35,37, nitro-neonicotinoid insecticide Flagship 25 myclobutanil37, and tebuconazole37 in honey bee [4A] WGNY†, mortality. In another study a 2.38-fold synergy with Platinum 75 myclobutanil at 24h, was detected in B. impatiens SGNY†, Cruiser mortality but not with difenoconazole. Synergizes 5FS with imazalil in both honey bees and bumble bees34. Thiamethoxam alone is highly toxic to bumble bees122,123 and some solitary bees124. Synergistic effect on honeybee mortality was detected when co-exposed to 125 thiamethoxam and Chronic Bee Paralysis Virus . thiamethoxam + Voliam See thiamethoxam and chlorantraniliprole separately for chlorantraniliprole FlexiNY†, synergy and toxicity information. NY nitro-neonicotinoid + Durivo † anthranilic diamide insecticide [4A+28] thiamethoxam + EndigoEPA†, See thiamethoxam and lambda-cyhalothrin separately lambda-cyhalothrin Endigo for synergy information. EPA/NY nitro-neonicotinoid + ZCX † pyrethroid insecticide [4A+3A] zeta-cypermethrin MustangEPA , See cypermethrin separately for synergy information. pyrethroid insecticide [3A] Mustang Zeta-cypermethrin is highly toxic to solitary bees52. MAXXEPA zeta-cypermethrin + GladiatorEPA See zeta-cypermethrin and avermectin separately for avermectin synergy and toxicity information. pyrethroid + avermectin insecticides [3+6]

22 Adjuvants, stickers, inert ingredients, and registered synergists Active Ingredient New York High Moderate Practically Synergies, sublethal effects, and toxicity to bee Chemical group Trade Name toxicity toxicity non-toxic species other than the honey bee [Resistance code] Examples N-methyl-2-pyrrolidone NMP is in This inert ingredient is highly toxic to honey bee larvae21. (NMP) abamectin inert ingredient often used in 0.15EC, pesticide formulations as a co- Ardent 0.15, solvent Exilis plus, Temprano non-ionic surfactant Induce, Honey bee learning ability was reduced by the non-ionic adjuvant LI-700, surfactant, Activator-9072. Regulaid organosilicone surfactant Phase, Increases susceptibility of bees to disease, resulting in adjuvant Silicone, exponentially increased mortality72,126. Silkin, Silt piperonyl butoxide (PBO) Ambush Synergizes with acetamiprid41, coumaphos20, cyfluthrin56, synergist Butacide, fenpyroximate20, lambda-cyhalothrin31,61, Exponent, permethrin106,31,60, prochloraz31,61, tau-fluvalinate20,56, PBO-8, and thiacloprid41 making these highly or more highly Pybuthrin, toxic than when applied alone. Coumaphos increased to Trilogy XL moderate toxicity with piperonyl butoxide. The product Ingredient in Advise® (imidacloprid) increased 5.2 fold in toxicity when Mustang combined with piperonyl butoxide, while the active MAXXEPA, and 92 ingredient imidacloprid alone was just 1.7x more toxic . other products polyethoxylated N-90, Sublethal effects on behavior of the honey bee in 72 Nonylphenol (N-90) Activator 90, response to the product Activator-90 as well as to Crossfire adjuvant managed solitary bee species when used alone and in the case of Grow-More® N-90, in combination with Rovral 4F® (iprodione) and Pristine® (pyraclostrobin + boscalid) which ultimately decreases reproductive 9 output .

*Please note that plant growth regulators (PGR’s) and herbicides are not included in this guide due to lack of research. However the few studies that have looked at some of these chemicals have found the obvious negative response of flora resource reduction.

©Heather Grab ©Katherine Urban-Mead

23 Literature Cited

1. McArt, S. H., Fersch, A. A., Milano, N. J., Truitt, L. L. & Boroczky, 14. Everich, R., Schiller, C., Whitehead, J., Beavers, M. & Barrett, K. K. High pesticide risk to honey bees despite low focal crop Effects of captan on Apis mellifera brood development under pollen collection during pollination of a mass blooming crop. field conditions in California almond orchards. J Econ Entomol Scientific Reports 7, 46554 (2017). 102, 20–29 (2009). 2. Fisher, A., Coleman, C., Hoffmann, C., Fritz, B. & Rangel, J. The 15. Ladurner, E., Bosch, J., Kemp, W. P. & Maini, S. Assessing synergistic effects of almond protection fungicides on honey delayed and acute toxicity of five formulated fungicides to bee (Hymenoptera: Apidae) forager survival. J Econ Entomol Osmia lignaria Say and Apis mellifera. Apidologie 36, 449–460 110, 802–808 (2017). (2005). 3. Schmuck, R., Stadler, T. & Schmidt, H.-W. Field relevance of a 16. Huntzinger, C. I., James, R. R., Bosch, J. & Kemp, W. P. synergistic effect observed in the laboratory between an EBI Laboratory bioassays to evaluate fungicides for chalkbrood fungicide and a chloronicotinyl insecticide in the honeybee control in larvae of the alfalfa leafcutting bee (Hymenoptera: (Apis mellifera L, Hymenoptera). Pest Management Science: Megachilidae). Journal of economic entomology 101, 660–667 formerly Pesticide Science 59, 279–286 (2003). (2008). 4. Mommaerts, V., Sterk, G., Hoffmann, L. & Smagghe, G. A 17. Huntzinger, C. I., James, R. R., Bosch, J. & Kemp, W. P. laboratory evaluation to determine the compatibility of Fungicide tests on adult alfalfa leafcutting bees (Hymenoptera: microbiological control agents with the pollinator Bombus Megachilidae). Journal of economic entomology 101, 1088– terrestris. Pest Management Science: formerly Pesticide Science 1094 (2008). 65, 949–955 (2009). 18. Malone, L. A., Scott‐Dupree, C. D., Todd, J. H. & Ramankutty, P. 5. Ramanaidu, K. & Cutler, G. C. Different toxic and hormetic No sub‐lethal toxicity to bumblebees, Bombus terrestris, responses of Bombus impatiens to Beauveria bassiana, Bacillus exposed to Bt‐corn pollen, captan and novaluron. New Zealand subtilis and spirotetramat. Pest management science 69, 949– Journal of Crop and Horticultural Science 35, 435–439 (2007). 954 (2013). 19. Thompson, H. & Wilkins, S. Assessment of the synergy and 6. Dedej, S., Delaplane, K. S. & Scherm, H. Effectiveness of honey repellency of pyrethroid/fungicide mixtures. B Insectol 56, bees in delivering the biocontrol agent Bacillus subtilis to 131–134 (2003). blueberry flowers to suppress mummy berry disease. Biological 20. Johnson, R. M., Dahlgren, L., Siegfried, B. D. & Ellis, M. D. Control 31, 422–427 (2004). Acaricide, fungicide and drug interactions in honey Bees (Apis 7. Tsvetkov, N. et al. Chronic exposure to neonicotinoids reduces mellifera). PLoS One 8, (2013). honey bee health near corn crops. Science 356, 1395–1397 21. Zhu, W., Schmehl, D. R., Mullin, C. A. & Frazier, J. L. Four (2017). common pesticides, their mixtures and a formulation solvent in 8. DeGrandi-Hoffman, G., Chen, Y. & Simonds, R. The effects of the hive environment have high oral toxicity to honey bee pesticides on queen rearing and virus titers in honey bees (Apis larvae. PLOS ONE 9, e77547 (2014). mellifera L.). Insects 4, 71–89 (2013). 22. vanEngelsdorp, D. et al. “Entombed Pollen”: A new condition in 9. Artz, D. R. & Pitts-Singer, T. L. Effects of fungicide and adjuvant honey bee colonies associated with increased risk of colony sprays on nesting behavior in two managed solitary bees, mortality. Journal of Invertebrate Pathology 101, 147–149 Osmia lignaria and Megachile rotundata. PLoS One 10, (2009). e0135688 (2015). 23. McArt, S. H., Urbanowicz, C., McCoshum, S., Irwin, R. E. & 10. Wade, A., Lin, C.-H., Kurkul, C., Regan, E. R. & Johnson, R. M. Adler, L. S. Landscape predictors of pathogen prevalence and Combined toxicity of insecticides and fungicides applied to range contractions in US bumblebees. Proc R Soc B 284, (2017). California almond orchards to honey bee larvae and adults. 24. Singh, N. Toxicity and compatibility of some commonly used Insects 10, 20 (2019). insectiicides with selected fungicides and herbicides against 11. Atkins, E. L. & Kellum, D. Comparative morphogenic and honey bee Apis mellifera L. (Govind Ballabh Pant University of toxicity studies on the effect of pesticides on honeybee brood. Agriculture and Technology; Pantnagar, 2003). Journal of Apicultural Research 25, 242–255 (1986). 25. Rodrigues, C. G., Krüger, A. P., Barbosa, W. F. & Guedes, R. N. 12. Mussen, E. C., Lopez, J. E. & Peng, C. Y. S. Effects of selected C. Leaf fertilizers affect survival and behavior of the fungicides on growth and development of larval honey bees, Neotropical stingless bee Friesella schrottkyi (Meliponini: Apis mellifera L. (Hymenoptera: Apidae). Environmental Apidae: Hymenoptera). J Econ Entomol 109, 1001–1008 (2016). Entomology 33, 1151–1154 (2004). 26. Vandame, R. & Belzunces, L. P. Joint actions of deltamethrin 13. Heylen, K., Gobin, B., Arckens, L., Huybrechts, R. & Billen, J. The and azole fungicides on honey bee thermoregulation. effects of four crop protection products on the morphology Neuroscience Letters 251, 57–60 (1998). and ultrastructure of the hypopharyngeal gland of the 27. Lefebvre, B. & Bassand, D. Bee selectivity of MAVRIK®(tau- European honeybee, Apis mellifera. Apidologie 42, 103–116 fluvalinate) in tank mix with ERIA®(Difenoconazole, Ergosterol (2011). Biosynthesis Inhibitor-EBI). Short, medium and long term effects under semi-fields conditions. COLLOQUES-INRA 71–78 (2001).

24 28. Iverson, A., Hale, C., Richardson, L., Miller, O. & McArt, S. 44. Steffan, S. A. et al. Empirical, Metagenomic, and Computational Synergistic effects of three sterol biosynthesis inhibiting Techniques Illuminate the Mechanisms by which Fungicides fungicides on the toxicity of a pyrethroid and neonicotinoid Compromise Bee Health. J. Vis. Exp. e54631 (2017) insecticide to bumble bees. Apidologie 50, 733–744 (2019). doi:doi:10.3791/54631 (2017). 29. Biddinger, D. J. et al. Comparative toxicities and synergism of 45. Zaluski, R., Justulin, L. A. & Orsi, R. de O. Field-relevant doses of apple orchard pesticides to Apis mellifera (L.) and Osmia the systemic insecticide fipronil and fungicide pyraclostrobin cornifrons (Radoszkowski). PLoS ONE 8, e72587 (2013). impair mandibular and hypopharyngeal glands in nurse 30. Albert, J. L. Field-level fungicide exposure and repellency to honeybees (Apis mellifera). Sci Rep 7, (2017). honey bees Apis mellifera during orchard bloom in Michigan. 46. Efrom, C. F. S., Redaelli, L. R., Meirelles, R. N. & Ourique, C. B. (Michigan State University, 2018). Side-effects of pesticides used in the organic system of 31. Pilling, E. D. Evidence for pesticide synergism in the honey bee production on Apis mellifera Linnaeus, 1758. Brazilian Archives (Apis mellifera). Aspects of Applied Biology 31, 43–47 (1992). of Biology and Technology 55, 47–53 (2012). 32. Pilling, E. D. & Jepson, P. C. Synergism between EBI fungicides 47. Tomé, H. V. V. et al. Agrochemical synergism imposes higher and a pyrethroid insecticide in the honeybee (Apis mellifera). risk to Neotropical bees than to honeybees. Royal Society Open Pesticide science 39, 293–297 (1993). Science 4, 160866 (2017). 33. European Food Safety Authority. Conclusion on the peer 48. Mullin, C. A. Effects of ‘inactive’ ingredients on bees. Curr Opin review of the pesticide risk assessment of the active substance Insect Sci 10, 194–200 (2015). flutriafol. EFSA Journal 8, 1868 (2010). 49. Carvalho, S. M., Carvalho, G. A., Carvalho, C. F., Bueno, C. F. & 34. Raimets, R. et al. Synergistic interactions between a variety of Baptista, A. P. M. Toxicity of acaricides/insecticides for citrus insecticides and an ergosterol biosynthesis inhibitor fungicide crop to the africanized honeybee Apis mellifera L. São Paulo 76, in dietary exposures of bumble bees (Bombus terrestris L.). Pest 597–607 (2009). Managment Science 74, 541–546 (2018). 50. Besard, L. et al. Compatibility of traditional and novel 35. DEFRA, R. and D. Assessing the impact of mixtures of acaricides with bumblebees (Bombus terrestris): a first pyrethroids and fungicides on honeybees. 1–20 laboratory assessment of toxicity and sublethal effects. Pest http://randd.defra.gov.uk/Document.aspx?Document=PN0945 Manag Sci 66, 786–93 (2010). _1951_FRP.doc (2004). 51. Devillers, J. et al. Comparative toxicity and hazards of 36. Camargo, C. Ecological risks of the conventional pesticides to Apis and non-Apis bees. A chemometrical study. insecticide/fungicide seed treatment mixture of thiamethoxam SAR QSAR Environ Res 14, 389–403 (2003). and mefenoxam in soybean on beneficial insects. (2016). 52. Uhl, P., Awanbor, O., Schulz, R. S. & Brühl, C. A. Osmia bicornis 37. Thompson, H. M., Fryday, S. L., Harkin, S. & Milner, S. Potential is rarely an adequate regulatory surrogate species. Comparing impacts of synergism in honeybees (Apis mellifera,) of its acute sensitivity towards multiple insecticides with exposure to neonicotinoids and sprayed fungicides in crops. regulatory Apis mellifera endpoints. bioRxiv 366237 (2018) Apidologie 45, 545–553 (2014). doi:10.1101/366237. 38. Sanchez-Bayo, F. & Goka, K. Pesticide residues and bees – a risk 53. Bendahou, N., Bounias, M. & Fleche, C. Acute toxicity of assessment. PLoS ONE 9, e94482 (2014). cypermethrin and on honeybees (Apis mellifera 39. Hawthorne, D. J. & Dively, G. P. Killing them with kindness? In- mellifera) according to age, formulations and (chronic paralysis hive medications may inhibit xenobiotic efflux transporters and virus)/insecticide interaction. J.Environ.Biol. 18, 55–65 (1997). endanger honey bees. PLOS ONE 6, e26796 (2011). 54. Barbosa, W. F., De Meyer, L., Guedes, R. N. C. & Smagghe, G. 40. Dinter, A., Scown, T., Deprez, C. & Hershberger, L. W. Lethal and sublethal effects of azadirachtin on the bumblebee Penthiopyrad (DPX-LEM17) 200 g/l SC and Penthiopyrad (DPX- Bombus terrestris (Hymenoptera: Apidae). Ecotoxicology 24, LEM17) 200 g/l EC - novel carboxamide fungicides with low 130–142 (2015). toxicity and low risk for beneficial non-target arthropods. 55. Mommaerts, V. & Smagghe, G. Side-effects of pesticides on the IOBC/WPRS Bulletin 82, 33–37 (2012). pollinator Bombus: an overview. (In-Tech, 2011). 41. Iwasa, T., Motoyama, N., Ambrose, J. T. & Roe, R. M. 56. Johnson, R. M., Wen, Z., Schuler, M. A. & Berenbaum, M. R. Mechanism for the differential toxicity of neonicotinoid Mediation of pyrethroid insecticide toxicity to honey bees insecticides in the honey bee, Apis mellifera. Crop Protection (Hymenoptera: Apidae) by cytochrome P450 monooxygenases. 23, 371–378 (2004). Journal of economic entomology 99, 1046–1050 (2006). 42. Sgolastra, F. et al. Synergistic mortality between a 57. Marletto, F., Patetta, A. & Manino, A. Laboratory assessment of neonicotinoid insecticide and an ergosterol-biosynthesis- pesticide toxicity to bumblebees. Bulletin of insectology 56, inhibiting fungicide in three bee species. Pest Management 155–158 (2003). Science 73, 1236–1243 (2017). 58. Fisher, A., Colman, C., Hoffmann, C., Fritz, B. & Rangel, J. The 43. Robinson, A. et al. Comparing bee species responses to effects of the insect growth regulators methoxyfenozide and chemical mixtures: common response patterns? PLOS ONE 12, pyriproxyfen and the acaricide bifenazate on honey bee e0176289 (2017). (Hymenoptera: Apidae) forager survival. J Econ Entomol 111, 510–516 (2018).

25 59. Ellis, M. D., Siegfried, B. D. & Spawn, B. The effect of Apistan® 76. Thompson, H. M., Wilkins, S., Battersby, A. H., Waite, R. J. & on honey bee (Apis mellifera L). Responses to methyl Wilkinson, D. The effects of four insect growth-regulating (IGR) , carbaryl and bifenthrin exposure. Apidologie 28, insecticides on honeybee (Apis mellifera L.) colony 123–127 (1997). development, queen rearing and drone sperm production. 60. Johnson, R. M., Pollock, H. S. & Berenbaum, M. R. Synergistic Ecotoxicology 14, 757–769 (2005). interactions between in-hive miticides in Apis mellifera. 77. Johnson, R. M. & Percel, E. G. Effect of a fungicide and spray Journal of Economic Entomology 102, 474–479 (2009). adjuvant on queen-rearing success in honey bees 61. Pilling, E. D., Bromleychallenor, K. A. C., Walker, C. H. & Jepson, (Hymenoptera: Apidae). J Econ Entomol 106, 1952–1957 P. C. Mechanism of synergism between the pyrethroid (2013). Insecticide λ-Cyhalothrin and the imidazole fungicide 78. Emmett, B. J. & Archer, B. M. The toxicity of diflubenzuron to prochloraz, in the honeybee (Apis mellifera L.). Pesticide honey bee (Apis mellifera L.) colonies in apple orchards. Plant biochemistry and physiology 51, 1–11 (1995). Pathology 29, 177–183 (1980). 62. Colin, M.-E. & Belzunces, L. P. Evidence of synergy between 79. Steen, J. J. M. van der. The effect of the size of the bumble bee prochloraz and deltamethrin in Apis mellifera L.: a convenient (Bombus terrestris L.) on the susceptibility to the pesticide biological approach. Pesticide Science 36, 115–119 (1992). dimethoate 40%. in Proceedings 7th international symposium 63. Johansen, C. A., Mayer, D. F., Eves, J. D. & Kious, C. W. of the ICPBR Bee Protection group: hazards of pesticides to bees Pesticides and Bees. 12, 6 (1983). at Universite d’Avignon, France, 07-09 Septembre 1999 213– 64. Kelley, A. G., Ling-Hsiu, L. & Berenbaum, M. You are what you 216 (2001). eat: food-drug interaction in honey bees (Apis mellifera). 80. Taséi, J.-N. & Dinet, P. Effets comparés de deux pyréthrinoides (2017). de synthèse et de trois insecticides organophosphorés sur les 65. Smagghe, G., Deknopper, J., Meeus, I. & Mommaerts, V. mégachiles (Megachile rotundata F.= pacifica Pz.). Apidologie Dietary chlorantraniliprole suppresses reproduction in worker 12, 363–376 (1981). bumblebees. Pest management science 69, 787–791 (2013). 81. Mayer, D. F., Lunden, J. D. & Kovacs, G. Susceptibility of four 66. Becker, R. Acute toxicity study on the impact of chlorpyrifos bee species (Hymenoptera: Apoidea) to field weathered and propiconazole in Apis mellifera. (University of Nebraska - insecticide residues. Journal of the Entomological Society of Lincoln, 2016). British Columbia 94, 27–30 (1997). 67. Wang, Y., Zhu, Y. C. & Li, W. Comparative examination on 82. Vidau, C. et al. Exposure to sublethal doses of fipronil and synergistic toxicities of chlorpyrifos, , or tetraconazole thiacloprid highly increases mortality of honeybees previously mixed with pyrethroid insecticides to honey bees (Apis infected by Nosema ceranae. PLoS one 6, e21550 (2011). mellifera L.). Environ Sci Pollut Res 27, 6971–6980 (2020). 83. Stanley, J., Sah, K., Jain, S. K., Bhatt, J. C. & Sushil, S. N. 68. Thompson, H. M. Assessing the exposure and toxicity of Evaluation of pesticide toxicity at their field recommended pesticides to bumblebees ( Bombus sp.). Apidologie 32, 305– doses to honeybees, Apis cerana and A. mellifera through 321 (2001). laboratory, semi-field and field studies. Chemosphere 119, 69. Gels, J. A., Held, D. W. & Potter, D. A. Hazards of insecticides to 668–674 (2015). the bumble bees Bombus impatiens (Hymenoptera: 84. Gradish, A. E., Scott-Dupree, C. D. & Cutler, G. C. Susceptibility Apidae) foraging on flowering white clover in turf. Journal of of Megachile rotundata to insecticides used in wild blueberry Economic Entomology 95, 722–728 (2002). production in Atlantic Canada. Journal of Pest Science 85, 133– 70. European Food Safety Authority, P., Italy. Conclusion on the 140 (2012). peer review of the pesticide risk assessment of the active 85. Gradish, A. E., Scott-Dupree, C. D., Frewin, A. J. & Cutler, G. C. substance cyantraniliprole. EFSA Journal 12, 3814 (2014). Lethal and sublethal effects of some insecticides recommended 71. Clinch, P. G. The residual contact toxicity to honey bees of for wild blueberry on the pollinator Bombus impatiens. The insecticides sprayed on to white clover (Trifolium repens l.) in Canadian Entomologist 144, 478–486 (2012). the laboratory. New Zealand Journal of Agricultural Research 86. Nation, J. L. & Robinson, F. A. Gibberellic acid: effects of 10, 289–300 (1967). feeding in an artificial diet for honeybees. Science 152, 1765– 72. Ciarlo, T. J., Mullin, C. A., Frazier, J. L. & Schmehl, D. R. Learning 1766 (1966). impairment in honey bees caused by agricultural spray 87. Marchetti, S., Barbattini, R. & D’AGARU, M. Comparative adjuvants. PLOS ONE 7, e40848 (2012). effectiveness of treatments used to control Varroa jacobsoni 73. Gupta, P. R. & Chandel, R. S. Effects of diflubenzuron and Oud. Apidologie 15, 363–378 (1984). penfluron on workers of Apis cerana indica F and Apis mellifera 88. Ellis, M. D. & Baxendale, F. P. Toxicity of seven monoterpenoids L. Apidologie 26, 3–10 (1995). to tracheal mites (Acari: Tarsonemidae) and their honey bee 74. Tasei, J.-N. Effects of insect growth regulators on honey bees (Hymenoptera: Apidae) hosts when applied as fumigants. and non-Apis bees. A review. Apidologie 32, 527–545 (2001). Journal of Economic Entomology 90, 1087–1091 (1997). 75. Abramson, C. I., Squire, J., Sheridan, A. & Mulder Jr, P. G. The effect of insecticides considered harmless to honey bees (Apis mellifera): proboscis conditioning studies by using the insect growth regulators tebufenozide and diflubenzuron. Environmental Entomology 33, 378–388 (2004).

26 89. Whittington, R., Winston, M. L., Melathopoulos, A. P. & Higo, 104. Mommaerts, V., Sterk, G. & Smagghe, G. Hazards and uptake of H. A. Evaluation of the botanical oils neem, thymol, and canola chitin synthesis inhibitors in bumblebees Bombus terrestris. sprayed to control Varroa jacobsoni Oud.(Acari: Varroidae) and Pest Management Science: formerly Pesticide Science 62, 752– Acarapis woodi (Acari: Tarsonemidae) in colonies of honey 758 (2006). bees (Apis mellifera L., Hymenoptera: Apidae). American Bee 105. Hodgson, E. W., Pitts-Singer, T. L. & Barbour, J. D. Effects of the Journal 140, 567–572 (2000). insect growth regulator, novaluron on immature alfalfa 90. Floris, I., Satta, A., Cabras, P., Garau, V. L. & Angioni, A. leafcutting bees, Megachile rotundata. J Insect Sci 11, (2011). Comparison between two thymol formulations in the control of 106. Hagler, J. R., Waller, G. D. & Lewis, B. E. Mortality of honeybees Varroa destructor: effectiveness, persistence, and residues. (Hymenoptera: Apidae) exposed to permethrin and Journal of economic entomology 97, 187–191 (2004). combinations of permethrin with piperonyl butoxide. Journal 91. Imdorf, A., Bogdanov, S., Ochoa, R. I. & Calderone, N. W. Use of of Apicultural Research 28, 208–211 (1989). essential oils for the control of Varroa jacobsoni Oud. in honey 107. Thompson, H. M. & Hunt, L. V. Extrapolating from honeybees bee colonies. Apidologie 30, 209–228 (1999). to bumblebees in pesticide risk assessment. Ecotoxicology 8, 92. Zhu, Y. C., Yao, J., Adamczyk, J. & Luttrell, R. Synergistic toxicity 147–166 (1999). and physiological impact of imidacloprid alone and binary 108. Piccolomini, A. M., Whiten, S. R., Flenniken, M. L., O’Neill, K. M. mixtures with seven representative pesticides on honey bee & Peterson, R. K. D. Acute toxicity of permethrin, deltamethrin, (Apis mellifera). PLoS One 12, e0176837 (2017). and to the alfalfa leafcutting bee. J Econ Entomol 93. Leza, M., Watrous, K. M., Bratu, J. & Woodard, S. H. Effects of 111, 1001–1005 (2018). neonicotinoid insecticide exposure and monofloral diet on 109. Appel, A. G. Knockdown efficiency and materials’ compatibility nest-founding bumblebee queens. Proc. R. Soc. B 285, of wasp and hornet spray formulations to honey bees 20180761 (2018). (Hymenoptera: Apidae). Journal of economic entomology 83, 94. Scott-Dupree, C. D., Conroy, L. & Harris, C. R. Impact of 1925–1931 (1990). currently used or potentially useful insecticides for canola 110. Fourrier, J. et al. Larval exposure to the juvenile hormone agroecosystems on Bombus impatiens (Hymenoptera: Apidae), analog pyriproxyfen disrupts acceptance of and social behavior Megachile rotundata (Hymentoptera: Megachilidae), and performance in adult honeybees. PLOS ONE 10, e0132985 Osmia lignaria (Hymenoptera: Megachilidae). Journal of (2015). Economic Entomology 102, 177–182 (2009). 111. Mommaerts, V., Sterk, G. & Smagghe, G. Bumblebees can be 95. Pashte, V. V. & Patil, C. S. Impact of different insecticides on used in combination with juvenile hormone analogues and the activity of bees on sunflower. Res Crops2017 18, 153–6 ecdysone agonists. Ecotoxicology 15, 513–521 (2006). (2017). 112. Besard, L., Mommaerts, V., Abdu‐Alla, G. & Smagghe, G. Lethal 96. Mayer, D. F., Kovacs, G. & Lunden, J. D. Field and laboratory and sublethal side-effect assessment supports a more benign tests on the effects of cyhalothrin on adults of Apis mellifera, profile of spinetoram compared with spinosad in the Megachile rotundata and Nomia melanderi. Journal of bumblebee Bombus terrestris. Pest Management Science 67, apicultural research 37, 33–37 (1998). 541–547 (2011). 97. Torchio, P. F. Relative toxicity of insecticides to the honey bee, 113. Abdu-Allah, G. A. M. & Pittendrigh, B. R. Lethal and sub-lethal alkali bee, and alfalfa leafcutting bee (Hymenoptera: Apidae, effects of select macrocyclic lactones insecticides on forager Halictidae, Megachilidae). Journal of the Kansas Entomological worker honey bees under laboratory experimental conditions. Society 446–453 (1973). Ecotoxicology 27, 81–88 (2018). 98. Caron, D. M. Effects of some ULV Mosquito 114. Mayes, M. A., Thompson, G. D., Husband, B. & Miles, M. M. Insecticides on Honey Bees12. Journal of Economic Entomology Spinosad toxicity to pollinators and associated risk. in Reviews 72, 148–151 (1979). of Environmental Contamination and Toxicology vol. 179 37–71 99. Drescher, W. & Geusen-Pfister, H. Comparative testing of the (Springer New York, 2003). oral toxicity of acephate, dimethoate and methomyl to 115. Morandin, L. A., Winston, M. L., Franklin, M. T. & Abbott, V. A. honeybees, bumblebees and syrphidae. in VI International Lethal and sub-lethal effects of spinosad on bumble bees Symposium on Pollination 288 133–138 (1990). (Bombus impatiens Cresson). Pest Manag Sci 61, 619–26 100. Naumann, K. & Isman, M. B. Toxicity of a neem (Azadirachta (2005). indica A. Juss) insecticide to larval honey bees. American Bee 116. Tomé, H. V. V., Barbosa, W. F., Martins, G. F. & Guedes, R. N. C. Journal (1996). Spinosad in the native stingless bee Melipona quadrifasciata: 101. Xavier, V. M. et al. Acute toxicity and sublethal effects of regrettable non-target toxicity of a bioinsecticide. botanical insecticides to honey bees. J Insect Sci 15, (2015). Chemosphere 124, 103–109 (2015). 102. González-Gómez, R. et al. Effects of neem () 117. Kang, M. & Jung, C. Ecotoxicology of several acaricides used in on honey bee workers and queens, while applied to control apple orchards to the honeybee, Apis mellifera : from the Varroa destructor. Journal of Apicultural Research 55, 413–421 laboratory to the field study. Journal of Apiculture 25, 155–161 (2016). (2010). 103. Cutler, G. C. & Scott-Dupree, C. D. Novaluron: prospects and 118. Baptista, A. P. M., Carvalho, G. A., Carvalho, S. M., Carvalho, C. limitations in insect pest management. Pest Technology 1.1 F. & Bueno Filho, J. S. de S. Toxicity of pesticides used in citrus (2007). crop to Apis mellifera. Ciência Rural 39, 955–961 (2009).

27 119. Ramanaidu, K. Blueberry spanworm, Itame argillacearia propiconazole, a DMI fungicide, on colony initiation in (Packard) and bumble bee, Bombus impatiens (Cresson) bumblebee (Bombus terrestris) micro-colonies. Apidologie 44, susceptibility to new biorational insecticides. (2011). 563–574 (2013). 120. Maus, C. Ecotoxicological profile of the insecticide 124. Sandrock, C. et al. Sublethal neonicotinoid insecticide exposure spirotetramat. Bayer CropScience Journal 23. reduces solitary bee reproductive success: Loss of pollinator 121. Ellis, C., Park, K. J., Whitehorn, P., David, A. & Goulson, D. The fitness. Agricultural and Forest Entomology 16, 119–128 neonicotinoid insecticide thiacloprid impacts upon bumblebee (2014). colony development under field conditions. Environ. Sci. 125. Coulon, M. et al. Metabolisation of thiamethoxam (a Technol. 51, 1727–1732 (2017). neonicotinoid pesticide) and interaction with the Chronic bee 122. Woodcock, B. A. et al. Country-specific effects of neonicotinoid paralysis virus in honeybees. Pesticide Biochemistry and pesticides on honey bees and wild bees. Science 356, 1393– Physiology 144, 10–18 (2018). 1395 (2017). 126. Fine, J. D., Cox-Foster, D. L. & Mullin, C. A. An inert pesticide 123. Elston, C., Thompson, H. M. & Walters, K. F. A. Sub-lethal adjuvant synergizes viral pathogenicity and mortality in honey effects of thiamethoxam, a neonicotinoid pesticide, and bee larvae. Scientific Reports 7, 40499 (2017).

An early spring solitary bee (Andrena sp.) collecting pollen from the anthers of an apple flower

28 Sample Pollination Services Contract

This sample contract is provided as a service and is not a substitute for legal advice.

This agreement dated ______is made between the following parties:

Beekeeper’s name: Grower’s name:

______

CONTACT INFORMATION Beekeeper Grower Mailing address: Phone number(s): Emergency phone number: Email address:

The parties agree to the following terms

CROP AND COLONY OVERVIEW This agreement involves the 20___ growing season Crop to be pollinated by honey bee colonies. This agreement is for crop varieties that are in flower. Address and/or GPS coordinates of orchard/field where the hives will be placed Date of colony placement* Date of colony removal* * If actual flowering dates differ from dates above, the grower will provide __ hours notice to the beekeeper regarding when colonies should be placed and removed No. of hives rented Price of a standard hive rental $ Total anticipated rental price Date(s) on which the rental fee is $ payable to the beekeeper Describe in detail or illustrate the colony placement in the orchard

The grower will provide right of entry at all times to beekeepers visiting the property so that s/he can Yes No manage colonies Before services are provided, the beekeeper will locate a holding yard to place colonies in the event Yes No that they require movement to avoid a pesticide spray A water source will be provided to the honey bee Beekeeper Grower colonies by the following party No water will be provided The grower and beekeeper agree to comply with all applicable federal, state and local laws, including pesticide label restrictions designed to protect bees.

The beekeeper agrees to provide colonies of the following standards:

COLONY STATUS OF A STANDARD HIVE Colony configuration (2 deeps, 1 deep, etc.) Minimum frames of bees in each hive Minimum frames of brood in each hive Pounds of food stores lbs Presence of a laying queen Colonies are free of American Foulbrood The beekeeper agrees to open and demonstrate the health and status of colonies randomly selected by the grower at least one (1) time following placement of the hives and thereafter as reasonably requested by the grower. The beekeeper will maintain colonies in good pollinating condition by providing feed, medication, and mite treatments as needed

This document was prepared by the Dyce Lab of Honey Bee Studies, Cornell University ©2018

29 The grower agrees to the following responsibilities:

GENERAL RESPONSIBILITIES The grower will provide a suitable place(s) for the hives that are accessible by truck or other vehicles The grower will hold the beekeeper harmless from any and all claims of injury or property damage arising from beekeeper’s performance of this contract, including but not limited to, claims arising from bee stings to animals or people, and claims for field or crop damage or loss resulting from the use of beekeepers vehicle(s).

MINIMIZING RISK OF PESTICIDE EXPOSURE The following pesticides or agricultural chemicals are mutually agreed to be used while the bees are on the crop: 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. The beekeeper will be notified of an application of a pesticide in this above list Yes No The beekeeper will be notified at the emergency contact (number/email address) provided above of an application of a pesticide that is not included in Yes No this above list The number of hours notice the grower agrees to give the beekeeper before a hrs pesticide is applied to a crop (e.g., 48 hrs) If a pesticide not included in the above list will be applied during pollination, the grower shall assume the costs to move the colonies away from and back to $ the crop. State the cost of moving colonies The grower will compensate the beekeeper for any colonies that died from acute pesticide poisoning events while present or within one month of pollinating this crop. Cause of death must be verified by the state apiculturist, $ state inspector, or Department of Environmental Conservation. State the cost of compensation per colony The grower will dispose of all pesticide products in a manner that bees will not be able to contact it while searching for a source of water

Additional agreements: ______

ADDITIONAL CONSIDERATIONS Prior to placing colonies for pollination, either party can terminate this contract should events occur beyond his/her control that prevent him or her from fulfilling the obligations as outlined (e.g., unexpected colony deaths, unexpected damage or disease of crops, etc.). If disputes arise that cannot be resolved through communication or small claims court, they will be settled by arbitration. Either party may request arbitration by providing written notice to the other at the contact information provided above by certified mail, return receipt requested. Within 10 days of receipt of such written request, each party will select one arbitrator and the two arbitrators will select a third. After reviewing the case, the decision of any two arbitrators will be binding. Cost of arbitration will be equally divided between the two parties. This contract shall be governed by New York law.

Signature of beekeeper: ______Date: ______

Signature of grower: ______Date: ______

This document was prepared by the Dyce Lab of Honey Bee Studies, Cornell University ©2018

30