Neurotoxic Pesticides and Behavioural Effects Upon Birds

Ecotoxicology, 12, 307±316, 2003 # 2003 Kluwer Academic Publishers. Manufactured in The Netherlands. Neurotoxic Pesticides and Behavioural Effects Upon Birds C. H. WALKER Cissbury, Hillhead, Colyton, Devon EX24 6NJ, UK Accepted 1 October 2002 Abstract. Organochlorine, organophosphorus, carbamate, pyrethroid and neonicotinoid insecticides and organomercuryfungicides are all neurotoxic and therefore have the potential to cause behavioural disturbances in birds. A number of studies have described behavioural effects caused to captive birds byneurotoxic pesticides, but it is verydifficult to measure such effects in the field, which is a serous limitation given their potential to cause adverse effects at the population level. The mode of action, and the neurotoxic and behavioural effects of these compounds are brieflyreviewed before considering evidence for their effects in the laboratoryand field. Behavioural effects maycause adverse changes at the population level either directlyor indirectly.Direct effects upon avian populations maybe due to disturbances of reproduction, feeding, or avoidance of predation. Indirect effects on predators maybe the consequence of direct action upon the preypopulation leading to either (1) reduction of numbers of the preypopulation, or (2) selective predation bythe predator upon the most contaminated individuals within the preypopulation. Attention is given to the historic evidence for neurotoxic and behavioural effects of persistent organochlorine insecticides, raising the question of retrospective analysis of existing data for this once important and intensively studied class of compounds. Less persistent pesticides currentlyin use mayalso have neurotoxic effects upon birds in the field. Sometimes, as with some OPs, their effects mayoutlast the persistence of their residues, and the ecotoxicityand persistence of some maybe affected byinteractions with other environmental chemicals. The development of new mechanistic biomarker assays could improve understanding of behavioural effects and possible associated effects at the population level caused bysuch compounds in the field. Keywords: neurotoxicity; pesticides; birds; behavioural effects; organochlorine insecticides; organophosphorus insecticides; organomercuryfungicides Introduction use of organophosphorus, carbamate and pyrethroid insecticides and the organomercuryfungicides because Since the early1960s and the publication of `Silent of established or perceived harmful effects upon Spring' byRachel Carson in 1962 much attention has animals in the field. It is noteworthythat the four main been given to the possible effects of pesticides upon groups of insecticides which are, or have been, widely birds and other vertebrates in the field. Evidence of used are all neurotoxic (Walker, 2001); the recently harmful effects of organochlorine insecticides such as developed neonicotinoids are also neurotoxic. It DDT, aldrin and dieldrin upon wild populations of appears that receptors within the nervous system predatorybirds contributed to the decision to impose present especiallyvulnerable targets not onlyfor man wide ranging bans on the use of these compounds made pesticides, but also for plant toxins that have worldwide. Restrictions have also been placed on the evolved during the course of `plant-animal warfare' 308 Walker (Harborne, 1993; Walker, 2001). Herbicides and varying considerably in their complexity and efficacy. fungicides, bycontrast, rarelyshow high toxicityto Unfortunatelysome of the tests which seemed animals. most relevant from an ecological point of viewÐfor The neurotoxic character of insecticides attracted example, on breeding behaviour, and capture of the attention and interest of behavioural biologists preyÐwere the most difficult to perform. In field working in the field of ecotoxicologyat an earlystage. studies it was particularlydifficult to identifybeha- Manykinds of physiological disturbances caused by vioural effects of environmental chemicals. Finally, exposure to pollutants could, in theory, lead to beha- he concluded that, although behavioural effects vioural changes but neurological disturbances seemed had been demonstrated down to doses one order of to be paramount importance. Alterations in the func- magnitude below those causing lethality, they were tion of the nervous system were very likely to be less sensitive than biochemical changesÐbiochem- expressed as changes in behaviour. Behavioural effects ical changes that could be incorporated into biomarker of pesticides were looked at from two related points of assays. view. On the one hand, toxicitytests working to beha- The present short review focuses on the possible vioural end points might present a sensitive means of ecological significance of behavioural effects caused testing for toxicityof environmental chemicals in an bypesticides. It draws on material from the above integrative way; that is, behavioural responses could review, and on discussions with David PeakallÐ represent an integrative measurement of lower level although interpretations are the responsibilityof the effects caused byone or several chemicals. The other author alone. point of view was that behavioural effects in the field might lead to population declines as a consequence of, for example, reduced abilityto find food or to repro- Ecological consequences of behavioural effects duce. The issue to emphasise here is that the useful- ness of the former approach is dependant on the Behaviour is here defined as the overt action an significance of the latter. The case for developing such organism takes to adjust to environmental circum- tests becomes a strong one if it can be shown that stance so as to ensure its survival (Odum, 1971). The pesticides cause population declines bybehavioural implementation of overt actions is a function of the mechanisms following realistic levels of exposure in nervous system, and the disruption of nervous function the field. byneurotoxic compounds maybe expected to cause An earlycontribution to this subject came from changes in behaviour. In the living environment, Warner et al. (1966), who developed a test system for pollutants maycause changes at the population level fish which utilised several behavioural parameters. becauseofDIRECT orINDIRECT behavioural effects. Theywere able to demonstrate changes in the beha- Direct effects maybe upon feeding, avoidance of pre- viour of goldfish caused bysublethal concentrations dation or reproduction or anycombination of these. of toxaphene (severe changes at 1.8 mg/l, more mild Adverse effects upon anyof these functions maylead effects at 0.44 mg/l). Toxaphene exerts neurotoxicity to population declines. Indirect effects upon predatory byacting upon GABA receptors. More recently, birds maybe due to pollutants having behavioural or Beauvais et al. (2000) have demonstrated behavioural other effects upon their prey. Thus, the decline of a changes in larval rainbow trout exposed to sublethal preyspecies caused bybehavioural effects maylead doses of the organophosphorus (OP) insecticides to a decline of the predator consequent upon a diazinon and malathion, even down to doses that reduction of food supply. An important consideration onlycaused 20% inhibition of brain cholinesterase. with putative behavioural changes caused bypollu- These and other studies have described assays for fish, tants in the field is the duration of the EFFECT. which can demonstrate behavioural changes at levels In theorypersistent neurotoxic compounds like of exposure well below lethal concentrations. A the organochlorine insecticides dieldrin and DDT critical and detailed review on the question of generallypresent a greater hazard than more biode- behavioural responses of birds to pesticides and gradable compounds such as organophosphorus, other environmental contaminants was published by carbamate or pyrethroid insecticides, because neuro- David Peakall (1985). He concluded that a wide toxic action is likelyto be much more prolonged. That varietyof behavioural tests had been tried in birds, said, there are some non-persistent compounds which Neurotoxicityin Birds 309 produce effects that outlast the compounds originally Mechanisms of neurotoxic action causing them, a point that will be returned to shortly. Considering direct effects upon feeding, these may Several different receptors within the nervous system be upon one or several different components of this are targets for the action of neurotoxic insecticides. activity(Atchison et al., 1996). Included here are Theyhave contrasting functions and locations within searching for, encountering, choosing, capturing and the peripheral and central nervous systems of verte- handling of prey. Learning and the functioning of the brates and invertebrates (Eldefrawi and Eldefrawi, sensorysystemare important in searching, encounter- 1990; Krieger et al., 2001). There are marked differ- ing and choosing. Capturing preymaysometimes be ences between species and groups in the form and verydifficult and involve highlyskilled hunting tech- distribution of these targets. In principle, the nature of niques and sophisticated coordination. Indeed, adverse behavioural effects caused byneurotoxic compounds effects of pollutants upon capturing and handling prey should depend on the type of receptor, and conse- have been demonstrated in a number of aquatic quentlythe mode(s) of action involved. The situation species (Atchison et al., 1996). Direct effects mayalso is complicated, however, bythe possibilityof differ- be

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