Replies to Reduced abundance of insects and spiders linked to radiation at Chernobyl 20 years after the accident — Biology Letters

2/28/11 11:21 AM

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AlertsGlobal change biology:
Anders Pape Møller and Timothy A. Mousseau
Reduced abundance of insects and spiders linked to radiation at Chernobyl
20 years after the accident
Biol. Lett. June 23, 2009 5:356-359; published online before print March 18, 2009,
doi:10.1098/rsbl.2008.0778

Abstract

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Rigorous methodology for studies of effects ofradiation from Chernobyl on animals and humans
Anders P. Møller, CNRS Researcher Timothy A. Mousseau
Université Paris-Sud XI

Wickliffe [1] recently criticized our research on the negative
association between abundance of invertebrates and levels ofradiation at Chernobyl [2], demanding information on (1) sampling
locations and blind research protocols, and (2) underlying
mechanisms that could account for the observed patterns.
We whole-heartedly subscribe to rigorous research approaches inany scientific endeavour. Our publication provided a map showing
the general locations of our study sites [2], and we would be happy
to provide GPS coordinates for the individual sites. We are unawareof any study reporting a large number of GPS coordinates forindividual study sites [e. g. 3-5], and we note that Wickliffe and hiscollaborators do not do so either (six publications cited in Wickliffe[1]), although that of course should not prevent others fromfollowing rigorous research protocols. Wickliffe [1] suggests that ourresearch findings may have been biased because they were notdone blindly. We note that this equally applies to research byWickliffe and co-workers (as cited in Wickliffe [1]), although theirlack of rigour should not prevent others from adopting more
rigorous methodology. For logistic reasons a double-blind approach
would be impossible at Chernobyl, at least for persons familiar withthe area. We have shown similar dose-dependent patterns ofradiation among years [6], and we have reported a significant
repeatability of census results among observers [7], suggesting that
there is no bias in our census results.
Wickliffe [1] argues that their studies on rodents have shown noeffects of radiation, prompting him to suggest that this should also
imply to other taxa such as invertebrates. We note that Wickliffe [1]only cites his own work and that of his collaborators showing 'noeffect' of radiation on rodents, while omitting to cite a single of themany publications by other scientists showing strongly negative
effects on chromosomal aberrations, lethality, embryo mortality andsterility [8-12], thus providing a biased view of available evidence.
How come that three different research groups working on rodents
in areas contaminated by radiation from Chernobyl show strongly
negative effects, while Wickliffe and collaborators show 'no effects'?
Finally, we note that while scientists working on rodents in the wild
adopt the internationally recognized rigorous approach of trap-lines
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Replies to Reduced abundance of insects and spiders linked to radiation at Chernobyl 20 years after the accident — Biology Letters2/28/11 11:21 AM

followed for two consecutive nights [e. g. 13], Wickliffe and coworkers have not adopted this standard practice to assess
abundance of rodents.
Finally, Wickliffe [1] suggests that without any knowledge ofunderlying mechanisms of radiation damage, there is no reason toconsider dose-dependent relationships as those that we reported[2]. We take issue with this approach to scientific investigations
because there is no priority when considering proximate andultimate scientific approaches to science [14]. Both approaches areequally valid, and both are required for developing a comprehensive
understanding of any biological or medical phenomenon. While
Wickliffe [1] dismisses any effects of low-dose radiation at the levels
we have investigated in Ukraine and Belarus, we notice that similar
or lower levels of radiation from Chernobyl, but also from nuclear
power plants in Germany, have had significant negative impacts onbirth rate and sex ratio in Germany [15-17], and on high school
attendance in Sweden [18].
To make progress on assessing the impacts of radiation from
Chernobyl on animals and humans, but also on other organisms, it
is imperative that we approach the questions while considering all
available information, and not just what fits into a specific mould.
Despite the Chernobyl accident happening 25 years ago, there is a
dearth of scientific information available, and what is available isoften not considered if it does not fit into a preconceived view of theeffects of radiation. We strongly urge scientists to help break thismould.
[1] Wickliffe, J.K., 2011. Clarification and explanation ofexperimental design and mechanistic dose-response effects for
significant radioecological impacts. Biology Letters el76.
[2] Møller, A.P., Mousseau, T.A. 2009. Reduced abundance ofinsects and spiders linked to radiation at Chernobyl 20 years after
the accident. Biology Letters 5, 356-359.
[3] Gregory, R.D., Willis, S.G., Jiguet, F., Vorisek, P., Klvanová, A.,
van Strien, A., Huntley, B., Collingham, Y.C., Couvet, D., Green,R.E. 2009. An indicator of the impact of climatic change on
European bird populations. Public Library of Science ONE 4(3),e4678.
[4] Jiguet, F., Julliard, R., Thomas, C.D., Dehorter, O., Newson,S.E., Couvet, D. 2006. Thermal range predicts bird resilience toextreme temperatures. Ecology Letters 9, 1321-1330.
[5] Schultz, S, Bradbury, R.B., Evans, K.L., Gregory, R.D.,
Blackburn, T.M. 2005. Brain size and resource specialization predict
long-term population trends in British birds. Proceedings of theRoyal Society of London B 272, 2305-2311.
[6] Møller, A.P., Mousseau, T.A. 2011. Efficiency of bio-indicatorsfor low-level radiation under field conditions. Ecological Indicators
11, 424-430.
[7] Møller, A.P., Mousseau, T.A. 2007. Species richness andabundance of birds in relation to radiation at Chernobyl. Biology
Letters 3, 483-486.
[8] Pomerantseva, M.D. et al. (1996) Genetic monitoring of housemice from regions polluted by radionuclides as the result of theChernobyl catastrophe. In Consequences of the Chernobyl

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Replies to Reduced abundance of insects and spiders linked to radiation at Chernobyl 20 years after the accident — Biology Letters

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Catastrophe: Environmental Health (Zakharov, V.M. and Krysanov,E.Y., eds), pp. 127-143, Center for Russian Environmental Policy.
[9] Pomerantseva, M.D., Ramaiya, L.K., Chekhovich, A.V. (1997)
Genetic disorders in house mouse germ cells after the Chernobyl
catastrophe. Mutation Research 381, 97-103.
[10] Shevchenko, V.A., Pomerantseva, M.D., Ramaiya, L.K.,
Chekhovich, A.V., Testov, B.V. (1992) Genetic disorders in mice
exposed to radiation in the vicinity of the Chernobyl nuclear powerstation. Science of the Total Environment 112, 45-56.
[11] Ryabokon, N.I., Smolich, I.I., Kudryashov, V.P., Goncharova,R.I. 2005. Long-term development of the radionuclide exposure ofmurine rodent populations in Belarus after the Chernobyl accident.
Radiation and Environmental Biophysics 44, 169-181.
[12] Ryabokon, N.I., Goncharova, R.I. 2006. Transgenerational
accumulation of radiation damage in small mammals chronically
exposed to Chernobyl fallout. Radiation and Environmental
Biophysics 45, 167-177.
[13] Steen, H., Ims, R.A., Sonerud, G.A. 1996. Spatial and temporalpatterns of small-rodent population dynamics at a regional scale.
Ecology 77, 2365-2372.
[14] Alcock, J., Sherman, P. 2010. The utility of the proximateultimate dichotomy in ethology. Ethology 96, 58-62.
[15] Scherb, H., Weigelt, E., Brüske-Hohlfeld, I. 2000. Regression
analysis of time trends in perinatal mortality in Germany 19801993. Environmental Health Perspectives 108, 159-165.
[16] Scherb, H., Voigt, K. 2007. Trends in the human sex odds atbirth in Europe and the Chernobyl Nuclear Power Plant accident.
Reproductive Toxicology 23, 593-599.
[17] Kusmierz, R., Voigt, K., Scherb, H. 2010. Is the human sex
odds at birth distorted in the vicinity of nuclear facilities (NF)? A
preliminary geo-spatial-temporal approach. In: K. Greve and A.B.
Cremers (eds). EnviroInfo 2010: Integration of Environmental
Information in Europe. Proceedings of the 24th International
Comnference on Informatics for Environmental Protection
Cologne/Bonn, Germany. Shaker Verlah, Aachen, Germany. Pp.
616-626.
[18] Almond, D., Edlund, L., Palmer, M. 2007. Chernobyl's
subclinical legacy: Prenatal exposure to radioactive fallout andschool outcomes in Sweden. National Bureau of Economic Research
13347, 1-50.

Conflict of Interest:
None declared... less
Published February 7, 2011

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Clarification and explanation of experimental
design and mechanistic dose-response effects for
significant radioecological impacts
Jeffrey K. Wickliffe, Assistant Professor Robert J. Baker, Horn
Professor
Tulane University, Texas Tech University

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Page 3 of 6Replies to Reduced abundance of insects and spiders linked to radiation at Chernobyl 20 years after the accident — Biology Letters

2/28/11 11:21 AM

The study on the detrimental effects of Chernobyl on insects byMoller and Mousseau represents a very interesting and unexpectedconclusion, which conflicts with the vast knowledge regarding
ionizing radiation effects and the principles of dose-response in thefield of toxicology and radiation biology. In addition, theexperimental design does not appear to hold to contemporary,rigorous standards.
As for the experimental design, two obvious problems are apparent
to us. The first is that the scientific observations and data collectedduring the field sampling were carried out by an individual that had
knowledge of the environmental conditions and "treatment" groups
during those periods. Pre-selected plots were assessed for insect
and avian presence and activity by a potentially biased observer
instead of an individual blinded to the environmental conditions
under study. This is particularly problematic in an ecological surveythat relies so heavily on the observer for results. Perhaps concern
for a blinded individual's safety and health was a primary concern.
That said, the lack of potential objectivity or some real, independentmeasure to guard against such bias should have been explicitlydeclared. In addition, information required to allow independent
replication of their study is inadequate. For example, no GPS or UTM
coordinates are given for their field sites. Therefore, it would beimpossible for an independent researcher to study these same sites.
This would seem to be an obvious shortcoming especially in a fieldbased ecological survey study.
As for the conclusions regarding the biological and ecologicalimpacts on insects, the authors should have explained the biologicalor radiotoxicological process by which such phenomenally low dose
rates can produce such "significant" effects. Dose-rates reported in
the published study are several orders of magnitude lower thanthose carefully reconstructed in several studies examining small
mammals within the exclusion zone, which have not found evidenceof biological, population genetic, or molecular genetic effects [1-6].
It is worth noting that the studies on mammals also find highlyvariable doses and dose-rates among specimens collected from thesame location [7-8]. Moller and Mousseau report apparent"biologically effective" radiation dose-rates that are essentiallyequivalent to radiation dose-rates human populations mightexperience living along the Gulf Coast of the United States (their low
radiation sites, 0.4uGy/hr) or those they may experience living on
the Colorado plateau and in the Rocky Mountain West (their highradiation sites, 0.6uGy/hr). These dose-rate estimates for U.S.
human population exposures are from the United States Nuclear
Regulatory Commission and the National Council on Radiation
Protection and Measurements. Recalling that insects, on average,
are relatively radioresistant in comparison to humans, would thisindicate that people living in high radiation sites in the U.S. are at asignificantly elevated health risk because of this almost
imperceptible increase in dose? The biological plausibility of thisconclusion is not obvious and, therefore, the authors should provide
a detailed, mechanism-based explanation for their findings. Is it
possible the results are "statistical" findings and not truly"biological" findings? We feel this last question should be addressedin the context of the rich and deep scientific literature on radiation
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Replies to Reduced abundance of insects and spiders linked to radiation at Chernobyl 20 years after the accident — Biology Letters

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genetics, radiation biology, and radioecology that does not tosupport their conclusions. It remains difficult to understand how thedramatic ecological changes brought about by the disaster, and theunprecedented exclusion of humans and human activity, do not
remain the best and strongest predictors of effects on invertebrate
and vertebrate populations. This is especially true in areas thatreceived negligible to very low levels of contamination.
For clearer answers to emerge from research conducted at
Chernobyl, rigorous experimental design and standards must beadhered to. In addition, apparent biological effects attributed solelyto radioactive contamination must have a logical, mechanistic
explanation derived to some extent from existing knowledge tosupport those conclusions.
1. Baker, R.J., Chesser, R., K., 2000. The Chornobyl nuclear disasterand subsequent creation of a wildlife preserve. Environmental
Toxicology and Chemistry 19, 1231-1232.
2. Baker, R.J., Hamilton, M.J., Bussche, R.A.v.D., Wiggins, L.E.,
Sugg, D.W., Smith, M.H., Lomakin, M.D., Gaschak, S.P., Bundova,E.G., Rudenskaya, G.A., Chesser, R.K., 1996. Small Mammals from
the Most Radioactive Sites near the Chornobyl Nuclear Power Plant.
Journal of Mammalogy 77, 155-170.
3. Meeks, H.N., Wickliffe, J.K., Hoofer, S.R., Chesser, R.K., Rodgers,B.E., Baker, R.J., 2007. Mitochondrial control region variation inbank voles (Clethrionomys glareolus) is not related to Chernobyl
radiation exposure. Environmental Toxicology and Chemistry 26,361-369.
4. Rodgers, B.E., Baker, R.J., 2000. Frequencies of micronuclei inbank voles from zones of high radiation at Chornobyl, Ukraine.
Environmental Toxicology and Chemistry 19, 1644-1648.
5. Rodgers, B.E., Wickliffe, J.K., Phillips, C.J., Chesser, R.K., Baker,R.J., 2001. Experimental exposure of naive bank voles(Clethrionomys glareolus) to the Chornobyl, Ukraine, environment:
A test of radioresistance. Environmental Toxicology and Chemistry20, 1936-1941.
6. Wickliffe, J.K., Chesser, R.K., Rodgers, B.E., Baker, R.J., 2002.
Assessing the genotoxicity of chronic environmental irradiation byusing mitochondrial DNA heterplasmy in the bank vole
(Clethrionomys glareolus) at Chornobyl, Ukraine. EnvironmentalToxicology and Chemistry 21, 1249- 1254.
7. Wickliffe, J.K., Dunina-Barkovskaya, Y.V., Gaschak, S.P.,
Rodgers, B.E., Chesser, R.K., Bondarkov, M., Baker, R.J., 2006.
Variation in mitochondrial DNA control region haplotypes in
populations of the bank vole, Clethrionomys glareolus, living in theChernobyl environment, Ukraine. Environmental Toxicology andChemistry 25, 503-508.
8. Chesser, R.K., Rodgers, B.E., Wickliffe, J.K., Gaschak, S.P.,
Chizhevsky, I., Phillips, C.J., Baker, R.J., 2001. Accumulation of137Cesium and 90Strontium from abiotic and biotic sources inrodents at Chornobyl, Ukraine. Environmental Toxicology andhttp://rsbl.royalsocietypublishing.org/content/5/3/356.abstract/reply#content-block

Page 5 of 6Replies to Reduced abundance of insects and spiders linked to radiation at Chernobyl 20 years after the accident — Biology Letters

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Chemistry 20, 1927-1935.
9. Chesser, R.K., Sugg, D.W., Lomakin, M.D., Bussche, R.A.v.d.,
DeWoody, J.A., Jagoe, C.H., Dallas, C.E., Whicker, F.W., Smith,M.H., Gaschak, S.P., Chizhevsky, I.V., Lyabik, V.V., Buntova, E.G.,
Holloman, K., Baker, R.J., 2000. Concentrations and dose rateestimates of 134137cesium and 90strontium in small mammals atchornobyl, Ukraine. Environmental Toxicology and Chemistry 19,305-312.

Conflict of Interest:
None declared... less
Published February 3, 2011

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