David M. Larson
Let's face it, we all can get lost, or at least a mite bewildered. Usually, the consequences are not dire—consult a map, check your phone or GPS device, even ask random strangers. But what happens when birds get lost, especially birds that migrate solo and at night? While we rarely know what happens to those lost wanderers, undoubtedly predation, starvation, and exposure all take their toll. You could argue that any bird that flies in the wrong direction on migration is an evolutionary dead end. But what if the problem is not with genetics but is caused by human intervention? What if one of the reasons is poisoning by pesticides?
Many environmental groups and governmental agencies have become increasingly worried about the effects of insecticides on birds, especially the commonly-used organophosphate and neonicotinoid compounds. Organophosphates such as chlorpyrifos (CPF) are usually scattered in granular form on crops, and neonicotinoids such as imidacloprid (IMI) are generally applied directly to seeds. Both are widely found in soil after application. Both classes of insecticides are neurotoxic: CFP is an acetylcholinesterase inhibitor and IMI is a nicotinic acetylcholine receptor antagonist.
An early study on White-throated Sparrows (Zonotrichia albicollis) during fall migration indicated that exposure to an organophosphate—acephate—caused a loss of migration orientation (Vyas, et al. 1995). Eng, et al. (2017) set out to test if White-crowned Sparrows (Zonotrichia leucophrys) showed impairments in weight gain or orientation ability—critical elements in migration—when exposed to environmentally relevant doses of imidacloprid and chlorpyrifos.
The authors captured White-crowned Sparrows during spring migration and fed them by gavage high (25% LD50) or low (10% LD50) doses of imidacloprid (IMI) or chlorpyrifos (CPF) or control (sunflower oil) once a day for three days. Both concentrations of IMI caused acute toxicity as indicated by statistically significant loss of body mass (average of 25.5% at high dose) during dosing. Treated birds also showed ataxia, lethargy, and excess salivation. None of the control birds died, but a small percent of the treated birds died or had to be euthanized. At the lower dose, the White-crowned Sparrows recovered weight by three days after treatment, and the high dose birds had normal weights after 14 days. In the CPF treatment groups, there were no obvious signs of acute toxicity—no distress, mortality, or weight loss significantly beyond control birds.
The researchers also tested migratory behavior in activity tests—cumulative distance moved via upward hops in Emlen funnels over 30 seconds. A classic Emlen funnel (Figure 1) is a white paper cone with a flat base that consists of an ink pad. Birds in migration restlessness— Zugunruhe—will hop from the base up onto the sides of the funnel, leaving ink marks in the preferred direction of travel. Eng and coworkers recorded activity and directional preference using video cameras rather than ink. Activity decreased over time in all groups, treated or control, and there was no significant difference between treated and control birds or between treatment groups.
Figure 1. Illustration of a classic Emlen funnel setup by the author.
Directionality of hopping was also scored. Pretreatment birds oriented generally northward (between 320° and 33°) as did the control-treated birds. Low-dose IMI-treated birds showed no orientation post-treatment but recovered their ability to orient by two weeks after treatment. High-dose birds changed from a northward orientation to a mean of 75°—so more easterly—post dosing, lost any orientation by three days after treatment, and recovered by two weeks. Birds treated with CPF, high or low dose, lost the ability to orient toward the north and did not recover by two weeks post treatment. Control birds maintained their northward orientation during the experimental period.
So, it seems that both IMI and CPF disrupt vital processes in spring migration in White-crowned Sparrows. For seed-eating birds that use agricultural habitats during migration, this is a particularly grim result. Grassland and agricultural species are among the fastest declining birds, and their susceptibility to these neurotoxins may be one of the reasons. Whether the disruption in migration is in orientation or in fitness, the net effect of these neurotoxins would be to reduce the likelihood of successful reproduction in affected birds.
The doses employed in this study are ones that could reasonably be encountered by birds in agricultural settings. The low IMI dose is equivalent to a White-crowned Sparrow consuming about four canola seeds or less than 10% of a corn seed, and the higher dose is about double that. Either of these amounts would be less than 1% of a bird's daily seed consumption. CPF consumption is mostly due to intake of granules as grit, which is a normal part of being a seedeater. The high and low doses of CPF in this study are equivalent to 8 or 12 granules of CPF, or perhaps 2.5–4 % of the grit ingested per day, based on a study on House Sparrows (Best and Gionfriddo 1994). Hence, it is highly possible for individual birds in a day's feeding to achieve doses of either neurotoxin as high or higher than those used in this study.
The question of the human toxicity of IMI is currently under review by the United States Environmental Protection Agency (see https://www.regulations.gov/docket?D=EPA-HQ-OPP-2008-0844). Effects of neonicotinoids on pollinators, other insects, other invertebrates, and non-human vertebrates are controversial, but this study is a notable step in outlining some of the problems with CFP and IMI exposure for seed-eating songbirds.
References
- Best, L.B., and J.P. Gionfriddo. 1994. House sparrow preferential consumption of carriers used for pesticide granules. Environmental Toxicology and Chemistry 13, 919–925.
- Eng, M.L., B.J. Stutchbury, and C.A. Morrissey. 2017. Imidacloprid and chlorpyrifos insecticides impair migratory ability in a seed-eating songbird. Nature Scientific Reports 7: 15176 (DOI:10.1038/s41598-017-15446-x).
- Vyas, N.B., E.F. Hill, J.R. Sauer, and W.J. Kuenzel. 1995. Acephate affects migratory orientation of the white-throated sparrow (Zonotrichia albicollis). Environmental Toxicology and Chemistry 14: 1961-5.
David M. Larson, PhD, is the Science and Education Coordinator at Mass Audubon's Joppa Flats Education Center in Newburyport, the Director of Mass Audubon's Birder's Certificate Program and the Certificate Program in Bird Ecology (a course for naturalist guides in Belize), a domestic and international tour leader, President of the Nuttall Ornithological Club, and a member of the editorial staff of Bird Observer..