The Effects of Sublethal Exposure to Diazinon, Carbaryl and Resmethrin on Longevity and Foraging in Apis Mellifera L K

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The effects of sublethal exposure to diazinon, carbaryl and resmethrin on longevity and foraging in Apis mellifera L K. E. Mackenzie, M. L. Winston

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K. E. Mackenzie, M. L. Winston. The effects of sublethal exposure to diazinon, carbaryl and resmethrin on longevity and foraging in Apis mellifera L. Apidologie, Springer Verlag, 1989, 20 (1), pp.29-40. hal- 00890761

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The effects of sublethal exposure to diazinon, carbaryl and resmethrin on longevity and foraging in Apis mellifera L.

K. E. MacKenzie M. L. Winston

Department of Biological Sciences, Center for Pest Management, Simon Fraser University, Burna- by, BC, Canada VSA 1 S6 (received 11-1-1988, accepted 31-7-1988)

Summary — Topical, sublethal applications of three insecticides, diazinon, carbaryl and resmethrin, were given to worker honey bees (Apis mellifera L.) of two age groups, 0 and 14 days. For newly emerged workers, carbaryl was the most hazardous in sublethal amounts, adversely affecting both longevity and foraging age. Resmethrin was intermediate in effect, and diazinon the least hazardous. This is different from mortality studies in which the effects of carbaryl and diazinon were similar, and resmethrin the most toxic. For 14-day-old workers, there were only two statistically significant differences affecting foraging in the sublethal studies, and these were not conclusive. However, in mortality studies carbaryl was the least toxic, diazinon intermediate and resmethrin the most toxic pesticide. Newly emerged worker honey bees were more sensitive to pesticide exposure, in both acute and sublethal effects, than older workers. In order to evaluate pesticide hazards to the honey bee, both laboratory and field tests should be used. A field bioassay involving sublethal exposure effects on longevity and foraging may be useful in this regard.

Apis mellifera— longevity - foraging - sublethal dose — insecticide

Résumé — Action de doses sublétales de diazinon, de carbaryl et de resméthrine sur la lon- gétivité et le butinage de l’abeille (Apis mellifica L.). On a montré que de petites quantités de pesticides pouvaient causer des eHets néfastes autant aux abeilles prises individuellement qu’à la colonie dans son ensemble. Cette étude évalue l’effet de l’exposition sublétale aux pesticides sur la longévité et le butinage des ouvrières de colonies standard de plein champ. On a fait des applications topiques sublétales de 3 insecticides, le diazinon, le carbaryl et la resméthrine, sur des ouvrières d’abeilles de deux groupes d’âge; 0 et 14 jours. On a testé les trois pesticides sur les abeilles naissantes et seulement le diazinon et le carbaryl sur les abeilles âgées de 14 jours. On a dilué chaque pesticide dans l’acétone pour obtenir des taux de mortalité d’environ 5, 10 et 25%, tels qu’ils sont déterminés dans les études de toxicité aigüe. Les ouvrières testées ont reçu 1 pl de la solution choisie et les témoins 1 ut d’acétone. La survie des ouvrières a été contrôlée tous les 10 à 14 jours. On a observé tous les troisièmes jours le butinage en bloquant l’entrée de la ruche pendant 30 minutes. Les abeilles testées trouvées hors de la ruche ont été classées comme butineuses. Les 3 colonies diffèrent significativement par la longévité et l’âge des butineuses (Tableau 11). Pour cette raison, dans les analyses suivantes les 3 colonies ont été considérées séparément. Pour les ouvrières naissantes, le carbaryl est le plus nocif aux doses sublétales, affectant à la fois la longévité et l’âge des butineuses (Tableau lit). La resméthrine a un effet intermédiaire et le diazinon est le moins nocif. Ces résultats sont différents de ceux obtenus avec la toxicité aigüe, pour laquelle le carbaryl et le diazinon produiseni des effets semblables et la resméthrine est la plus toxique (Tableau I). Chez les ouvrières âgées de 14 jours, on n’a trouvé que 2 différences statistiquement significa- tives pour les doses sublétales, mais elles ne sont pas concluantes (Tableau IV). Toutefois, en ce qui concerne la toxicité aigüe, la carbaryl s’est montré le moins toxique, le diazinon d’effet intermé- diaire et la resméthrine la plus toxique (Tableau 1). Les relations entre les 3 insecticides ne sont pas les mêmes dans les tests de toxicité aigüe et dans les tests des effets sublétaux. La resméthrine, qui a la toxicité aigüe la plus élevée, produit des effets sublétaux moindres que ceux du carbaryl, qui a la toxicité aigüe la plus faible. Les ouvrières naissantes sont plus sensibles aux pesticides que les ouvrières plus âgées, tant dans les effets sublétaux qu’aigus. Afin d’évaluer la toxicité des pesticides pour les abeilles, il est nécessaire de faire des tests à la fois au laboratoire et sur le terrain. A cette fin, un test biologique prenant en compte les effets d’une exposition sublétale sur la longévité et le butinage serait utile.

Apis mellifica - longévité - butinage - dose sublétale - insecticide

Zusammenfassung — Wirkung subletaler Dosen von Diazinon, Carbaryl und Resmethrin auf Langlebigkeit und Sammelaktivität bei der Honigbiene (Apis mellifera L.). Auch geringe Men- gen von Pestiziden zeigen oft zerstörerische Wirkungen sowohl auf die einzelne Biene als auch auf die Kolonie als Ganzes. In dieser Untersuchung sollte der Einfluß von subletalen Dosen von Pesti- ziden auf die Langlebigkeit und das Sammelverhalten von Arbeitsbienen in Standard-Freilandvöl- kern beurteilt werden. Arbeitsbienen (Apis mellifera) aus zwei verschiedenen Altersgruppen (0 und 14 Tage alt) wurden mit subletalen Dosen von 3 Insektiziden (Diazinon, Carbaryl und Resmethrin) topikal behandelt. Alle drei Chemikalien wurden bei frisch geschlüpften Arbeitshienen getestet, aber nur Diazinon und Carbaryl bei den 14 Tage alten Bienen. Jedes Insektizid wurden in Aceton aufgelöst, und zwar so, daß Mortalitätsstufen von ungefähr 5%, 10°/ und 25% vorgegeben waren, die aus Untersuchungen der akuten Toxizität bestimmt wurden. Die Testhienen erhielten 1 pl der jeweiligen Konzentration und die Kontrollbienen 1 pl Aceton. Die Überlebensrate der Arbeiterinnen wurde 10- 14täglich kontrolliert. An jedem dritten Tag wurde die Sammelaktivität protokolliert. Dazu wurde das Flugloch für 30 min geschlossen. Testhienen, die sich außerhalb des Stockes einfanden, wurden als Sammlerinnen gezählt. Die drei in diesem Versuch verwendeten Kolonien unterschieden sich signifikant in der Langle- bigkeit und im Sammelalter (Tab. 11). Dehalb wurden die drei Völker bei den folgenden Analysen separat betrachtet. Bei frisch geschlüpften Bienen war Carbaryl in subletalen Dosen das gefähr- lichste Gitt. Es wirkte sich nachteilig sowohl auf die Langlebigkeit als auch auf das Sammelalter aus (Tab. III). Resmethrin war im Effekt ein mittelmäßiges und Diazinon das am wenigsten gefährliche Gitt. Dies war bei den Tests über die akute Giftwirkung anders, dort waren Carbaryl und Diazinon gleich und Resmethrin das gefährlichste Gift (Tab. I). Bei 14 Tage alten Bienen ergab die Untersuchung der Wirkung von subletalen Dosen nur zwei statistisch signifikante Unterschiede und diese waren nicht schlüssig (Tab. IV). Jedoch war bei der Untersuchung der akuten Wirkung Carbaryl das am wenigsten gittige, Diazinon ein mittelmäßiges und Resmethrin das gittigste Agens (Tab. 1). Das Verhältnis der drei Insektizide bei der Untersuchung der akuten Giftwirkung war also ver- schieden vom Verhältnis bei subletalen Dosen. Resmethrin, das am meisten akut gittige, hatte weniger nachteilige Effekte als Carbaryl, das am wenigsten akut gittige. Frisch geschlüptte Bienen waren empfindlicher gegen Pestizide als ältere Bienen, sowohl bei akuten wie bei subletalen Gitt- wirkungen. Um die Gefährlichkeit von Pestiziden zu beurteilen, sollten daher Labor- und Feldver- suche durchgeführt werden. Ein Bioassay zur Untersuchung der Effekte subletaler Dosen auf die Langlebigkeit und das Sammelverhalten wäre sinnvoll.

Apis mellifera - Langlebigkeit - Sammelaktivität - subletale Dosen — Insektizide Introduction acute toxicity and sublethal effects of a pesticide when gauging its hazard to the The honey bee (Apis mellifera L.) is honey bee. recognized as our most important crop A bioassay using longevity as a meas- pollinator (McGregor, 1976; NRCC, 1981; ure to evaluate sublethal pesticide expo- Crane and Walker, 1983). North American sure to the honey bee has been sugges- agricultural products valued at some $ 20 ted (Smirle et aL, 1984). This study was billion (U.S.) depend in some way on the designed to examine the sublethal effects honey bee (Levin, 1984; Winston and of three insecticides, and to evaluate the Scott, 1984). Pesticide use has also be- effect of treatment age on the results. In come an essential part of modern agricul- addition to longevity, foraging was also ture, and the honey bee is susceptible to studied, since increasing foraging activity many commonly used chemicals (Ander- and earlier foraging age have both been son and Atkins, 1968; Atkins, 1975; correlated with reduced longevity (Free Johansen, 1977, 1979, 1983; NRCC, and Spencer-Booth, 1959; Sekiguchi and 1981 It is important, therefore, to under- Sakagami, 1966; Winston and Katz, 1981, stand how to protect this pollinator from 1982; Winston and Fergusson, 1985). pesticide exposure and to evaluate the Inclusion of this task, foraging, may hazards different chemicals pose. increase the sensitivity of the bioassay. A number of different factors should be considered when pesticides are evaluated for their hazard to the bee. Acute honey Materials and Methods toxicity studies which assess mortality have been used almost exclusively in these considerations. However, exposure Chemicals to sublethal concentrations of pesticides Commercial formulations of the three insecti- in the field also could have adverse cides were used. The organophosphorous effects on colony success, honey produc- insecticide diazinon was formulated as a 12.5% tion and emulsifiable concentrate (Later’s Diazinon, crop pollination (NRCC, 1981). PCP Act. No. 11437, Later Chemicals Ltd., Chronic of such used feeding commonly Richmond, BC), the carbamate carbaryl as a pesticides as acephate (Stoner et al., 22.5% concentrate (Wilson Liquid Sevin Car- 1985), carbaryl (Winterlin and Walker, baryl insecticide, PCP Act. No. 17971, Wilson 1973), dimethoate (Waller and Barker, Laboratories Inc., Dundas, Ontario), and the resmethrin as a 0.25% solution Waller et Barker et pyrethroid 1979; al., 1979; al., (House Plant Insect Killer, PCP Act. No. 16219, 1980; Stoner et al., 1983) and carbofuran Later Chemicals Ltd., Richmond, BC). The for- (Stoner et al., 1982) to whole colonies mulations were diluted in acetone to the requir- reduced honey production, brood rearing ed concentrations. The formulation of carbaryl and worker size. Sublethal was first diluted (1:10) with distilled water to population facilitate further mixing with acetone. topical treatments to individual workers resulted in impairment in the dance lan- guage with methyl-parathion (Schricker The colonies and Stephen, 1970), reduced lifespan with Test colonies were located at Simon Fraser malathion or diazinon (Smirle et al., 1984; University, Burnaby, BC and studies conducted MacKenzie, 1986); and altered foraging from June to September 1985. Workers to be treated were obtained from a with diazinon single colony (not patterns (MacKenzie, 1986) one of the experimental colonies) to minimize and permethrin (Cox and Wilson, 1984). It genetic variation. Combs containing emerging is important therefore to evaluate both workers were placed overnight in an incubator at 34°C and 50—70% RH. Newly emerged doses corresponding to the desired mortality workers were marked on the dorsal surface of levels. the thorax with coloured and numbered plastic For experimental purposes, newly emerged labels Chr. Craze, KG, (Opalithplattchen, honey bee workers (0 days of age) were treat- Endersbach, FRG), and either treated immed- ed with all 3 pesticides, while 14-day old work- or introduced into a test hive and remov- iately ers were treated with diazinon and carbaryl ed and treated at the desired age. only, due to time constraints. This left a number Three colonies in standard Langstroth deep of untreated workers, exposed to neither pest- equipment were used. These colonies consis- icide nor acetone, in each of the 3 colonies. ted of 2 boxes (supers) with 10 frames each, Newly emerged bees were treated on 18—20 enough workers to cover most of the frames, June with the desired dosage of pesticide, and and a healthy laying queen. A third super was placed in the hive through the feeding hole in added 10 July to alleviate colony crowding. the top board. Treatments for the 14-day old This super was removed on 16 August for bees were carried out on 3 July for colonies 1 honey extraction. Experimentation began 18 and 3, and 4 July for colony 2. The hives were June and continued until 5 September for col- taken apart and frames examined one by one. onies 1 and 3, and 1 August for colony 2. Marked workers were picked up by the hind Queen problems occured in colonies 1 and 3. leg, treated, held in a cage until all treatments Colony 1 was found to be queenless on 100 for the hive were completed, and reintroduced August and was requeened on 16 August. A through the feeding hole. The number of wor- virgin queen was found and removed from kers treated per dose ranged from 50-65. colony 3 on 27 June. Subsequently, the original queen appeared to be laying normally, but was superseded sometime before 18 July. Observations Entrance observations began on 22 June and continued every third day until most of the bees Treatments were dead. Entrances were blocked with wire screen for 15 min, any workers from Honey bee workers were treated with a preventing topical or then the numbers of mark- insecticide application on the dorsal surface of leaving entering, ed workers at the entrance were recorded for their abdomens. An SMI Micro/Peftor-AO was another 15 min. All workers were used to 1 treatment solution to returning dispense pl considered to be and each insect. Workers were held the hind foragers (Winston Katz, by leg 10—14 the colonies were with while the insecticide was 1982). Every days forceps applied. checked for workers and A of workers were treated with 1 acet- surviving by removing group wl each frame and one as a control in all Concentra- examining carefully recording experiments. all marked workers. tions causing approximately 5%, 10% and 25% mortalities were used for each pesticide and each age group in the sublethal experiments. Data analyses Acute toxicity tests for the 3 chemi- (LD50) Acute data were the cals were conducted to choose the dose range toxicity analyzed using WHO method for insecticide tests for sublethal exposure. Between 40 to 50 work- susceptibility ers were treated at each of the 4 to 7 doses in (Swaroop, 1966). The criterion of nonoverlap- the mortality tests. Newly emerged workers (0 ping 95% confidence limits was used to deter- mine differences between for days) were treated and into holding significant LD50s placed each cages, while the older age group (14 days) was age group. marked at emergence, placed into standard For sublethal studies, longevity and the first colonies, removed at the appropriate age day and duration of foraging were analyzed. (grasped by their hind legs with forceps and Longevity in days was determined as the mid- placed into cages) immobilized with carbon point between the last day seen and the subse- dioxide and treated, and placed into holding quent day survivorship was examined. Forag- cages. Sugar syrup (50%) and water were sup- ing was considered to commence on the first plied ad libitum via gravity feeding bottles. Mor- day a worker was seen outside the hive in the tality counts were taken at 24 h and data anal- entrance observations. Duration of foraging yzed following the WHO for insecticide was the number of days between the first and susceptibility tests (Swarrop, 1966). The result- last time a worker was seen outside the hive. ant regression lines were used to calculate The treated controls and the 3 dosages of each pesticide in each age group initially were com- and diazinon to be of similar toxicity pared by one-way analysis of variance and and resmethrin the more toxic Duncan’s test Then acutely multiple range (Zar, 1984). The between the 3 to examine the effects of different pesticides, all (Table I). relationships pesticide treatments in one age group were chemicals for the 14-day old workers analyzed by two-way analysis of variance (i.e., were : carbaryl was the least toxic pest- pesticide and dosage) and the Student—New— icide, resmethrin the most, with diazinon man—Keuls test multiple comparison (Zar, in between. In addition, all chemicals were 1984). , found to be more To evaluate the effects of differ- significantly acutely possible toxic to workers than 14- ences in colony conditions, data from the mark- newly emerged ed, untreated workers in the colonies were day old workers. compared by one-way analysis of variance and untreated workers in the 3 test Student-Newman-Keuls Marked, multiple comparison colonies were different in lon- test (Zar, 1984) for each of the 3 categories significantly examined. gevity and the first day of foraging (Table II). Colonies 1 and 2 were similar in duration of foraging, but statistically different from colony 3. Therefore, further anal- Results yses of sublethal data were carried out separately for the 3 colonies. Acute toxicity tests of the 3 chemicals to Sublethal exposure to carbaryl had newly emerged workers showed carbaryl adverse effects on longevity and foraging in newly emerged workers (Table 111). In Discussion colonies 1 and 2, control workers lived longer than those treated with carbaryl, This has evaluated both lethal and and began foraging later in colony 1 and paper sublethal effects of 3 different insecticides earlier in colony 2. In colony 3, the only on the bee. was found to significant difference between control and honey Carbaryl be more harmful to work- pesticide-treated bees was that bees newly emerged ers than diazinon or resmethrin in sub- treated with carbaryl LD25 continued fora- lethal resmethrin was the ging longer than either of the other 2 tests, although most acutely toxic pesticide. There were dosages or the control. few effects on 14-day old workers in When the toxicities of all 3 pesticides sublethal experiments; but once again, in were for work- compared newly emerged acute tests resmethrin was the most toxic, ers, caused more adverse effects carbaryl while carbaryl was the least toxic insect- than the other two chemicals, with a icide. These toxicity rankings are the general pattern of decreased in longevity same as those previously published all 3 and the latest in colonies, foraging (NRCC, 1981), and all 3 chemicals have 1 was inter- colony (Table 111). Longevity been placed into groups with high hazard mediate in bees treated with resmethrin, to the honey bee 1979; Crane and in those treated (Johansen, longer with diazinon. and Walker, 1983). There were no effects on foraging due to In hazard to resmethrin or diazinon treatment. rating pesticide honey bees, acute toxicity values of mortality are When workers were treated at 14 days often relied on (Anderson and Atkins, of with or diazinon, there age carbaryl 1968; Atkins, 1975; Johansen, 1977; were 2 statistically different results (Table NRCC, even when field The control continued 1981), exper- IV). group foraging imentation is into the hazard than treatment in col- incorporated longer any carbaryl The between chem- 2. In earliest rating. relationships ony colony 3, foraging began icals in and field stud- in those workers treated with diazinon laboratory mortality ies have been shown to in some LD5, latest in those treated with carbaryl vary cases. For example, the synthetic pyre- LD5, and was intermediate in the other throids, such as permethrin, have high treatment groups. acute toxicities in mortality tests and are In this study the relationships between of low hazard in the field due to low appli- acute toxicity and sublethal effects also cation rates and repellent action (Pike varied. Resmethrin, the most acutely toxic et al., 1982; Shires et aL, 1984). compound, was only intermediate in its sublethal effects, while carbaryl, which regulating temporal division of labour than caused the most sublethal effects in this pesticide exposure, which makes uncov- study, was not the most acutely toxic. Car- ering sublethal pesticide effects difficult. baryl has been found to be a serious Newly emerged workers were found to problem for beekeepers, causing high be more sensitive to pesticides, mortality to field colonies (Johansen and including both acute toxicity and sublethal expo- Brown, 1972; Anderson and Glowa, 1984; sure, than older workers. P,revious studies Melksham et al., 1985). In studies on resi- on acute toxicities agree with this result dual of 10 pesticides, was toxicity carbaryl (Koch, 1958/1959; and Burk- rated as the most hazardous to Mayland honey hardt, 1970; Smirle et aL, 1984; Mac- bees due to its persistence (Mansour ett Kenzie, 1986). Differences in toxicities al., 1984; Mansour and Al-Jalili, 1985). could be related to a number of factors, These 2 characteristics, adverse effects of including differences in enzyme levels or sublethal and a residual nature, exposure activities and absorptivity of the cuticle. may account for the beekeeping problems Other insects have been found to be more caused by carbaryl. These results suggest susceptible after moults and at emerg- that, in addition to and field laboratory ence which sublethal stud- (Busvine, 1971). Enzymes experimentation, exposure metabolize xenobiotics are found in the ies should be used when the rating bee. Smirle and Winston hazards of chemicals to the bee. honey (1988) honey found that the concentrations and acti- Foraging and longevity are both cat- vities of 2 important detoxification that have egories been shown to be enzymes, glutathione S-transferases and affected sublethal by exposure to pesti- the polysubstrate monooxygenases, were cides (MacKenzie, 1986; and this study). very low in newly emerged workers com- and are Foraging longevity related, since pared to any other age from 1 to 7 weeks. earlier foraging activity results in reduced This alone could account for the great lifespan (Free and Spencer-Booth, 1959; susceptibility of newly emerged workers to Sekiguchi and Sakagami, 1966; Winston various insecticides. and Fergusson, 1985). Reduced longevity Stress also have been a factor in was a more consistent indicator of ad- may this verse sublethal pesticide exposure than study. Honey bees, especially newly are sensitive to stress age of first foraging, but neither of these emerged workers, in forms such as narcosis categories were affected in all cases. many (Beck- Considering the number of factors, includ- mann, 1974; Ebadi et al., 1980), sublethal ing worker activity, internal colony condi- pesticide exposure (Schricker and Ste- tions and forage availability (Maurizio, phen, 1970; Smirle et al., 1984), and 1950; Woyke, 1984; Winston and Fergus- increased activity (Lindauer, 1953; Free and and neural son, 1985), that can influence lifespan Spencer-Booth, 1959), and foraging in the honey bee, perhaps function has been shown to be adversely affected some of these and this is to be expected. In an earlier study, by (Stephen Smirle et al. (1984) also found reduced Schricker, 1970; Beckmann, 1974). As the longevity due to sublethal pesticide 3 insecticides used in this study are all nervous neural exposure. Similar results were obtained system poisons, impairment be involved in both the lethal due to single sublethal exposure to diazi- may and sublethal effects found. non in observation hives (MacKenzie, 1986). Probably other factors are more This work suggests that an insecticide important in determining longevity and has both lethal and sublethal effects, which do not necessarily have the same pollen contamination in alfalfa treated with relationship for each chemical. In dimethoate. Arch. Environ. Contam. Toxicol. 9, rating 125-133 pesticide hazards to the honey bee, a bio- Beckmann H.E. des sublethal effects should (1974) Beeinflussung assay involving Geddchtnisses der Honigbiene durch Narkose, be considered in addition to acute toxi- Kiihlung und Strefi. J. Comp. Physiol. 94, cities studies in the laboratory and the 249-266 field. Longevity and foraging appear to be Busvine J.R. (1971) A Critical Review of the potential measures to use in the develop- Techniques for Testing Insecticides. Common- wealth Bureau, UK ment of such a bioassay, although more Agricultural Slough, work remains to be done to refine this Cox R.L. & Wilson W.T. (1984) Effects of permethrin on the behaviour of individually tagged Evaluation of a wider of technique. range honey bees, Apis mellifera L. (Hymenoptera : pesticides, including herbicides and fungi- Apidae). Environ. EntomoL 13, 375-378 cides, should be made, and the relation- Crane E. & Walker P. (1983) The Impact of ship between acute and sublethal pest- Pest Management on Bees and Pollination. icide effects on the individual and the Tropical Development and Research Institute, colony studied. London, UK Ebadi R., Gary N.E. & Lorenzen K. (1980) Effects of carbon dioxide and low temperature narcosis on honey bees, Apis mellifera. Envi- ron. Entomol. 9, 144-149 Acknowlegments Free J.B. & Spencer-Booth Y. 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