Fipronil: Pest Control and Ecosystem Conservation Alex Brooks-Schrauth

At the dawning of the twenty-first century, the number of environmental challenges the world faces is astonishing from industrial wastes, water and air contamination, loss of biodiversity and unsustainable use of natural resources. Well before todays extremes, in 1987, the World Commission on Environment and Development recognized the ever increasing risks and set a goal to meet the needs of the present without compromising the ability of future generations to meet their own needs.i Major factors in this debate are food security and health assurance. Since man began living in agrarian communities there has been a constant struggle to support the ever increasing population with greater amounts of food. Crop pests can pose a significant threat to production. Pests, such as insects, can also infest the home; becoming a nuisance and possible harbinger of disease. In an effort to curb these vexations, risks and production barriers, science has utilized a myriad of chemicals to halt the march of invaders. One increasingly popular insecticide of late is Fipronil. Fipronil has the ability to insure food security, comfort at home, and reduce disease risks; but what may we be trading for these assurances? Insecticides have a long history of use, but within recent decades, due to concerns of environmental or toxic effects, they have been rapidly evolving and changing. Chlorinated insecticides, such as DDT with discovery of detrimental reproductive effects, were replaced by organophosphates and carbamates. Concerns over their toxicity lead to staunch restrictions on their uses and replacement by pyrethroids, which have been partially replaced by Fipronil; manufactured under such trade names as Frontline, Combat, Regent, and Icon among others. Fipronil(Figure 1) is a phenylpyrazole insecticide, whose mode of action targets GABA, blocking the voltage gated chloride channels.ii Preventing chlorine uptake by the CNS causes excessive neuronal stimulation and eventual death of the target insect. Fipronil originally gained favor as it has a higher binding affinity for insect neuronal receptor complexes, and thus a higher selectivity and safety margin. Fipronil has a variety of formulations from roach and ant bait traps, tick and flea spotons or spray for pets, to granular pesticide treatments for crops. It has proven highly effective in control of locusts that afflict crops in semi-arid and arid environments. Its use was a large factor in suppressing a locust plague in Madagascar, which began in 1997 and lasted roughly three years. The devastation of croplands triggered large-scale control operations, consisting of fullcover spraying in the region.iii As opposed to pests that develop in close association with the host crop and require local pesticide applications, locusts necessitate control in perimeter natural landscapes.iv Such usage means that diverse environmental populations are exposed to the treatment chemical. Intricate, naive ecosystems such as these are not adapted to the pesticide and

may suffer severe perturbations. Though Fipronil was proven to have a higher safety margin than many other pesticides in laboratory experiments, as is so often the case, the world proved it was not such a controlled environment. Very effective locust control was achieved, but not without direct, and indirect, detrimental effects on many species. In addition to the locusts that inundate the arid environments, termites have prevalent populations in the areas. Knowing that, a study was undertaken in Madagascar during 2000 to determine the effects on exposed termite colonies and their relation to indigenous vertebrates. Fipronil was found to cause a high level of reduction in termite numbers, nearly 50%, and in one case 80%, in sprayed plots. Solely thought of as a pest within developed areas, the termite is a keystone species within many natural environments; removing detritus, contributing to nutrient cycling within the soil, and representing a substantial dietary component of local vertebrates. Being relatively abundant within the study area, the lizard Chalarodon madagascariensis and the lesser hedgehog, Echinops telfairi, were monitored. The lizard population was found to experience significant decline, also near 50%, on fipronil plots, while the hedgehog became absent from the plots, but remained frequent in unsprayed plots and plots treated with an alternate pesticide. v The study presented strong evidence for vertebrate species food chain stress imposed by the application of fipronil(Figure 2 Non target effects of fipronil exposure. Arid environments in Australia suffer from similar locust concerns and are dealt with via the aerial application of fipronil. After conducting studies of fipronil impacts on indigenous wildlife populations relating to ant and termite populations, they found that the numbers and diversity of termite species directly correlated with vertebrate diversity and population numbers. With these results brought to their attention, the Australian Plague Locust Commission (APLC) drafted new regulations of fipronil applications. Blanket treatments of fipronil are no longer allowed, instead, applications must have broad barrier widths in order to limit ecosystem exposure. To ensure such regulations are followed, planes/pilots applying the pesticide must be registered with the APLC and outfitted with a GPS to record locations of treatment and ensure great enough barrier width. vi Food depletion is not the only effect on local wildlife. Direct exposure can have far reaching disturbances on reproduction and thriftiness of vertebrates, as has been demonstrated in a study of egg laying finches and hens. Crop growth, therefore fipronil application, coincides with the peak breeding season of many species; greatly increasing the probability of exposure to off-spring and their mothers. Groups of zebra finches were given varying doses of fipronil during their breeding/laying cycle and their exposure and that of their chicks/eggs were determined afterwards. Of the eggs laid, only 14% hatched, that being from the lowest dose group, and the off-spring exhibited severe underdevelopment and reduced feeding behavior in contrast to control chicks, which had 100% hatchability.vii Fipronil and its sulfone metabolites, or fiproles, were found in the brain, liver, adipose tissue, and yolks, in line with the lipophilic nature of the compound. Of importance, is the finding that the biological metabolite, which is maternally transferred, fipronil-sulfone is twenty times more active at vertebrate chloride gated channels

than insects. Though birds will clearly not be directly administered fipronil in the wild, there are numerous ways they may be exposed through their diet. Birds can eat their body weight in 48 hours and can easily reach these experimental doses through natural consumption. It has been found that fipronil contaminated locusts survive for 7-10 days after exposure.viii During this time, many a hungry bird has the opportunity to consume them. In addition, fipronil remains on the plants and seed coats for some time after application, allowing for consumption of the compound by not only insectivorous birds, but granivorous birds also.ix Negative effects are not only reserved to remote arid environments, but are being discovered in our own backyards. Fipronil is an increasingly popular household and garden insecticide and its growing use is evident within our water ways. A survey of residential water run-off in California showed high contamination of fipronil and its derivatives.x High enough levels to warrant concern over its ecotoxicological affects. Initial studies pointed to the increased safety margin if fipronil, but emerging evidence shows its metabolites to have a greater toxic affect and be of a greater concern than the parent compound. The photometabolite fipronildesulfinyl is ten times more active at mammalian chloride channels than insects.xi This photoproduct represents the majority of contribution to the measured fiproles in the water. It has been demonstrated to be several times more lethal to vertebrates and aquatic organisms. Further, before its registration as an urban pesticide treatment, fipronil was used in the southern United States for protection against pests in rice fields. This application and subsequent discharge was linked to an unprecedented mortality of crawfish.xii In home use is not limited to keeping pesky ants out of the kitchen, but is utilized in keeping the family pet healthy happy and healthy, also. Spot-on formulations of fipronil, such as Frontline, are of common use within households with pets to reduce/eliminate flea and tick burdens. Such application is generally considered safe, but some precautions need be heeded. Due to their unique metabolism and GI conformation, fipronil is not to be used on rabbits as it causes extreme neurotoxic effects and death. Its application on dogs and cats is generally unremarkable outside of possibly being a cause of pruritus or alopecia.xiii Off-label usage has an increased incidence of adverse effects, such as neurological toxicity (generally with recovery) and individual variations in sensitivity have been noted even with recommended dosing, requiring a recommended monitoring of pets after initial applications. Accidental ingestion, via licking, in dogs and cats may cause fipronil poisoning with CNS hyperexcitibility, tremors, and seizures.xiv Outside of the above instances, fipronil has had unforeseen negative effects on many aquatic copepods, fish, and tree frogs, and is a probable contributing factor in honey bee colony collapse disorder.xv xvi xvii Such consequences of the use of fipronil are disturbing and do not bode well for the environment and wildlife populations, but this is not to say that fipronil use ought to be ceased. It has proven to be highly effective in assuring crop vigor and food safety in arid regions and as a household pest control. Compared to its predecessors, it is remarkably safe. Such results and safety margins are impressive, but they are meaningless in the long run if our

environment is slowly being poisoned and biodiversity is ever decreasing with its applications. Continual monitoring of fipronil use, and its metabolites effects, must continue, if not expand. More regulations ensuring the least amount of exposure must be put in place. The negative effects of fiproles are just now being elucidated, and indirect stressors seem to have a lagged effect, further complicating our ability to reach a more complete understanding of the adverse effects. There will never be a day when insecticides are not used to ensure food production or the comforts of home, but a product must do more good than harm for its use to be warranted. Reduction of detrimental chemical exposure to ecosystems may be more easily achieved in urban environments, but in areas with limited crop land and reduced resources, achieving a balance of pest control and ecosystem health will prove more difficult as hungry people do not worry about long reaching effects in a far off tomorrow. Pest control and protection of diverse ecosystems tend to be seen as mutually exclusive, but they need not be. As chemicals evolve, so must we, in our recognition of a couple of simple principles, as Ralf Peveling puts it, the genuine human right of people to save their crops and the inherent value of other life-forms beyond their potential as a resource.xviii

Figure 1 Two dimensional structure of Fipronil

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Figure 2 Non target effects of fipronil exposure

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"A/RES/42/187 Report of the World Commission on Environment and Development." UN News Center. UN, 16 Dec. 1989. Web. 20 April 2012. <http://www.un.org/documents/ga/res/42/ares42-187.htm>. ii Nahri-Niknafs, Babbak, and Abbas Ahmadi. "Simulated Solar Light Irradiation of Fipronil in Natural Waters in North of Iran and Identification of Photoproducts by GC-MS."Electronic Journal of Environmental, Agricultural and Food Chemistry 10.7 (2011): 2560-567. iii Peveling, R., A. N. McWilliam, P. Nagel, H. Rasolomanana, Raholijaona, L. Rakotomianina, A. Ravoninjatovo, C. F. Dewhurst, G. Gibson, S. Rafanomezana, and C. C. D. Tingle. "Impact of Locust Control on Harvester Termites and Endemic Vertebrate Predators in Madagascar." Journal of Applied Ecology 40.4 (2003): 729-41. iv Peveling, Ralf. "Environmental Conservation and Locust Control Possible Conflicts and Solutions." Journal of Orthoptera Research 10.2 (2001): 171-87. v Peveling, R. et al (2003) 729. vi Steinbauer, M.j., and R. Peveling. "The Impact of the Locust Control Insecticide Fipronil on Termites and Ants in Two Contrasting Habitats in Northern Australia." Crop Protection 30.7 (2011): 814-25. vii Kitulagodage, Malsha, William A. Buttemer, and Lee B. Astheimer. "Adverse Effects of Fipronil on Avian Reproduction and Development: Maternal Transfer of Fipronil to Eggs in Zebra Finch Taeniopygia Guttata and in Ovo Exposure in Chickens Gallus Demesticus." Ecotoxicology 20.Feb (2011): 653-60. viii EPA. Assessment of the Impact of Insecticide Spraying of Australian Plague Locusts. Environment Protection Agency, Department for the Environment and Heritage, Government of South Australia. Adelaide, Australia. 2001. ix JMPR. Pesticide Residues in Food: Fipronil 2001 evaluations. Part I, FAO Plant Production and Protections Paper. Joint Meeting on Pesticide Residues: FAO and WHO.171. Web. 18 Apr. 2012. < http://www.fao.org/ag/AGP/AGPP/Pesticid/JMPR/Download/2001_eva/00%20Table%20of%20Contents.pdf>. x Gan, J., S. Bondarenko, L. Oki, D. Haver, and J. X. Li. "Occurence of Fipronil and Its Biologically Active Derivatives in Urban Residential Runoff." Environmental Science and Technology 46 (2012): 1489-495. xi Nahri-Niknafs, Babak, et al.2564. xii Bedient, Philip B., Randy D. Horsak, Dan Schlenk, Rik M. Hovinga, and Julia D. Pierson. "Environmental Impact of Fipronil to the Louisiana Crawfish Industry."Environmental Forensics 6.3 (2005): 289-99. xiii Australian Pesticides and Veterinary Medicines Authority. Safety of Fipronil in Dogs and Cats: a review of literature. 9.

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Gupta, Ramesh C. "Chapter 43 Fipronil." Veterinary Toxicology: Basic and Clinical Principles. New York: Elsevier, 2007. 502-04. xv Gupta, Ramesh C. "Chapter 43 Fipronil." Veterinary Toxicology: Basic and Clinical Principles. New York: Elsevier, 2007. 502-04. xvi Krger, Robert, and Matthew T. Moore. "Chemical Residence Time and Hydrological Conditions Influence Treatment of Fipronil in Vegetated Aquatic Mesocosms."Journal of Environment Quality 40.2 (2011): 559-65. xvii Pareja, Lucia, Marcos Colazzo, Perez-Parada Andres, Silvina Niell, Leonidas Carrasco-Letelier, Natalia Besil, Maria Veronica Cesio, and Horacio Heinzen. "Detection of Pesticides in Active and Depopulated Beehives in Uruguay." Int. J. Environmental Research and Public Health 8 (2011): 3844-858. xviii Peveling, Ralf. (2001). 183 xix "Fipronil - Compound Summary." Fipronil - PubChem. NCBI. Web. 18 Apr. 2012. <http://pubchem.ncbi.nlm.nih.gov/summary/summary.cgi?cid=3352>. xx Peveling, Ralf. (2001). 180.