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Developmental lead exposure has mixed effects on butterfly cognitive processes

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Abstract

While the effects of lead pollution have been well studied in vertebrates, it is unclear to what extent lead may negatively affect insect cognition. Lead pollution in soils can elevate lead in plant tissues, suggesting it could negatively affect neural development of insect herbivores. We used the cabbage white butterfly (Pieris rapae) as a model system to study the effect of lead pollution on insect cognitive processes, which play an important role in how insects locate and handle resources. Cabbage white butterfly larvae were reared on a 4-ppm lead diet, a concentration representative of vegetation in polluted sites; we measured eye size and performance on a foraging assay in adults. Relative to controls, lead-reared butterflies did not differ in time or ability to search for a food reward associated with a less preferred color. Indeed, lead-treated butterflies were more likely to participate in the behavioral assay itself. Lead exposure did not negatively affect survival or body size, and it actually sped up development time. The effects of lead on relative eye size varied with sex: lead tended to reduce eye size in males, but increase eye size in females. These results suggest that low levels of lead pollution may have mixed effects on butterfly vision, but only minimal impacts on performance in foraging tasks, although follow-up work is needed to test whether this result is specific to cabbage whites, which are often associated with disturbed areas.

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References

  • Ali FA (1974) Structure and metamorphosis of the brain and suboesophageal ganglion of Pieris brassicae (L.) (Lepidoptera: Pieridae). Trans R Entomol Soc Lond 125:363–412

    Article  Google Scholar 

  • Blackiston D, Briscoe AD, Weiss MR (2011) Color vision and learning in the monarch butterfly, Danaus plexippus (Nymphalidae). J Exp Biol 214:509–520

    Article  PubMed  Google Scholar 

  • Blumstein DT, Evans CS, Daniel JC (2006) JWatcher v. 1.0. See www.jwatcher.ucla.edu

  • Burden CM, Elmore C, Hladun KR et al (2016) Acute exposure to selenium disrupts associative conditioning and long-term memory recall in honey bees (Apis mellifera). Ecotoxicol Environ Saf 127:71–79

    Article  CAS  PubMed  Google Scholar 

  • Burger J (1998) Effects of lead on sibling recognition in young herring gulls. Toxicol Sci 43:155–160

    Article  CAS  PubMed  Google Scholar 

  • Burger J, Gochfeld M (1993) Lead and behavioral development in young herring gulls: effects of timing of exposure on individual recognition. Toxicol Sci 21:187–195

    Article  CAS  Google Scholar 

  • Burger J, Gochfeld M (2005) Effects of lead on learning in herring gulls: an avian wildlife model for neurobehavioral deficits. Neurotoxicology 26:615–624

    Article  CAS  PubMed  Google Scholar 

  • Byzitter J, Lukowiak K, Karnik V, Dalesman S (2012) Acute combined exposure to heavy metals (Zn, Cd) blocks memory formation in a freshwater snail. Ecotoxicology 21:860–868

    Article  CAS  PubMed  Google Scholar 

  • Calabrese EJ, Baldwin LA (2002) Defining hormesis. Hum Exp Toxicol 21:91–97. doi:10.1191/0960327102ht217oa

    Article  CAS  PubMed  Google Scholar 

  • Cecil KM, Brubaker CJ, Adler CM et al (2008) Decreased brain volume in adults with childhood lead exposure. PLoS Med 5:e112

    Article  PubMed  PubMed Central  Google Scholar 

  • Cepero LC, Rosenwald LC, Weiss MR (2015) The relative importance of flower color and shape for the foraging monarch butterfly (Lepidoptera: Nymphalidae). J Insect Behav 28:499–511

    Article  Google Scholar 

  • Chittka L, Raine NE (2006) Recognition of flowers by pollinators. Curr Opin Plant Biol 9:428–435

    Article  PubMed  Google Scholar 

  • Daneshparvar M, Jeddi MZ, Yunesian M et al (2016) The role of lead exposure on attention-deficit/hyperactivity disorder in children: a systematic review. Iran J Psychiatry 11:1–14

    PubMed  PubMed Central  Google Scholar 

  • Datko-Williams L, Wilkie A, Richmond-Bryant J (2014) Analysis of US soil lead (Pb) studies from 1970 to 2012. Sci Total Environ 468:854–863

    Article  PubMed  Google Scholar 

  • Dell'aglio DD, Losada ME, Jiggins CD (2016) Butterfly learning and the diversification of plant leaf shape. Front Ecol Evol 4:81

    Article  Google Scholar 

  • Eisler R (1988) Lead hazards to fish, wildlife, and invertebrates: a synoptic review. US Fish and Wildlife Service, Laurel

    Google Scholar 

  • Ethier A-A, Muckle G, Bastien C et al (2012) Effects of environmental contaminant exposure on visual brain development: a prospective electrophysiological study in school-aged children. Neurotoxicology 33:1075–1085. doi:10.1016/j.neuro.2012.05.010

    Article  CAS  PubMed  Google Scholar 

  • Feeny P, Städler E, Åhman I, Carter M (1989) Effects of plant odor on oviposition by the black swallowtail butterfly, Papilio polyxenes (Lepidoptera: Papilionidae). J Insect Behav 2(6):803–827

    Article  Google Scholar 

  • Finster ME, Gray KA, Binns HJ (2004) Lead levels of edibles grown in contaminated residential soils: a field survey. Sci Total Environ 320:245–257

    Article  CAS  PubMed  Google Scholar 

  • Flora G, Gupta D, Tiwari A (2012) Toxicity of lead: a review with recent updates. Interdiscip Toxicol 5:47–58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garza A, Vega R, Soto E (2006) Cellular mechanisms of lead neurotoxicity. Med Sci Monit 12:RA57–RA65

    PubMed  Google Scholar 

  • Gintenreiter S, Ortel J, Nopp HJ (1993a) Effects of different dietary levels of cadmium, lead, copper, and zinc on the vitality of the forest pest insect Lymantria dispar L. (Lymantriidae, Lepid). Arch Environ Contam Toxicol 25:62–66

    CAS  Google Scholar 

  • Gintenreiter S, Ortel J, Nopp HJ (1993b) Bioaccumulation of cadmium, lead, copper, and zinc in successive developmental stages of Lymantria dispar L. (Lymantriidae, Lepid)—a life cycle study. Arch Environ Contam Toxicol 25:55–61

    CAS  Google Scholar 

  • Goodlad JK, Marcus DK, Fulton JJ (2013) Lead and attention-deficit/hyperactivity disorder (ADHD) symptoms: a meta-analysis. Clin Psychol Rev 33:417–425

    Article  PubMed  Google Scholar 

  • Gorissen L, Snoeijs T, Van Duyse E, Eens M (2005) Heavy metal pollution affects dawn singing behaviour in a small passerine bird. Oecologia 145:504–509

    Article  PubMed  Google Scholar 

  • Goulson D, Cory JS (1993) Flower constancy and learning in foraging preferences of the green-veined white butterfly Pieris napi. Ecol Entomol 18:315–320

    Article  Google Scholar 

  • Harrison R (2012) Lead pollution: causes and control. Springer, Berlin

    Google Scholar 

  • He T, Hirsch HVB, Ruden DM, Lnenicka GA (2009) Chronic lead exposure alters presynaptic calcium regulation and synaptic facilitation in Drosophila larvae. Neurotoxicology 30:777–784. doi:10.1016/j.neuro.2009.08.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heinze S, Reppert SM (2012) Anatomical basis of sun compass navigation I: the general layout of the monarch butterfly brain. J Comp Neurol 520:1599–1628

    Article  PubMed  Google Scholar 

  • Hern A, Edwards-Jones G, McKinlay RG (1996) A review of the pre-oviposition behaviour of the small cabbage white butterfly, Pieris rapae (Lepidoptera: Pieridae). Ann Appl Biol 128:349–371

    Article  Google Scholar 

  • Hirsch HV, Mercer J, Sambaziotis H et al (2003) Behavioral effects of chronic exposure to low levels of lead in Drosophila melanogaster. Neurotoxicology 24:435–442

    Article  CAS  PubMed  Google Scholar 

  • Hirsch HV, Possidente D, Averill S et al (2009) Variations at a quantitative trait locus (QTL) affect development of behavior in lead-exposed Drosophila melanogaster. Neurotoxicology 30:305–311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hogsden KL, Hutchinson TC (2004) Butterfly assemblages along a human disturbance gradient in Ontario, Canada. Can J Zool 82:739–748

    Article  Google Scholar 

  • Kandori I, Ohsaki N (1996) The learning abilities of the white cabbage butterfly, Pieris rapae, foraging for flowers. Res Popul Ecol 38:111–117

    Article  Google Scholar 

  • Kenig B, Stamenković-Radak M, Andelković M (2013) Population specific fitness response of Drosophila subobscura to lead pollution. Insect Sci 20:245–253. doi:10.1111/j.1744-7917.2012.01501.x

    Article  CAS  PubMed  Google Scholar 

  • Khan A, Khan S, Khan MA et al (2015) The uptake and bioaccumulation of heavy metals by food plants, their effects on plants nutrients, and associated health risk: a review. Environ Sci Pollut Res 22:13772–13799

    Article  CAS  Google Scholar 

  • Kim S, Arora M, Fernandez C et al (2013) Lead, mercury, and cadmium exposure and attention deficit hyperactivity disorder in children. Environ Res 126:105–110

    Article  CAS  PubMed  Google Scholar 

  • Kocher SD, Williams EH (2000) The diversity and abundance of North American butterflies vary with habitat disturbance and geography. J Biogeogr 27:785–794

    Article  Google Scholar 

  • Kuester A, Conner JK, Culley T, Baucom RS (2014) How weeds emerge: a taxonomic and trait-based examination using United States data. New Phytol 202:1055–1068. doi:10.1111/nph.12698

    Article  PubMed  PubMed Central  Google Scholar 

  • Kusano T, Sato H (1980) The sensitivity of tarsal chemoreceptors for sugars in the cabbage butterfly, Pieris rapae crucivora Boisduval. Appl Entomol Zool 15(4):385–391

    CAS  Google Scholar 

  • Laverty TM, Plowright RC (1988) Flower handling by bumblebees: a comparison of specialists and generalists. Anim Behav 36:733–740

    Article  Google Scholar 

  • Lewis AC (1986) Memory constraints and flower choice in Pieris rapae. Science 232:863–865

    Article  CAS  PubMed  Google Scholar 

  • Luo M, Xu Y, Cai R et al (2014) Epigenetic histone modification regulates developmental lead exposure induced hyperactivity in rats. Toxicol Lett 225:78–85

    Article  CAS  PubMed  Google Scholar 

  • Lynn SK, Cnaani J, Papaj DR (2005) Peak shift discrimination learning as a mechanism of signal evolution. Evolution 59:1300–1305

    Article  PubMed  Google Scholar 

  • Margulies C, Tully T, Dubnau J (2005) Deconstructing memory in Drosophila. Curr Biol 15(17):R700–R713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mason LH, Harp JP, Han DY (2014) Pb Neurotoxicity: neuropsychological effects of lead toxicity. BioMed Res Int 2014:8. doi:10.1155/2014/840547

    Google Scholar 

  • Massadeh A, Al-Momani F, Elbetieha A (2008) Assessment of heavy metals concentrations in soil samples from the vicinity of busy roads: influence on Drosophila melanogaster life cycle. Biol Trace Elem Res 122:292–299

    Article  CAS  PubMed  Google Scholar 

  • Mitchell RG, Spliethoff HM, Ribaudo LN et al (2014) Lead (Pb) and other metals in New York City community garden soils: factors influencing contaminant distributions. Environ Pollut 187:162–169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morley EJ, Hirsch HVB, Hollocher K, Lnenicka GA (2003) Effects of chronic lead exposure on the neuromuscular junction in Drosophila larvae. NeuroToxicology 24:35–41. doi:10.1016/S0161-813X(02)00095-5

    Article  CAS  PubMed  Google Scholar 

  • Ômura H, Honda K (2004) Priority of color over scent during flower visitation by adult Vanessa indica butterflies. Oecologia 142:588–596. doi:10.1007/s00442-004-1761-6

    Article  PubMed  Google Scholar 

  • Papaj DR, Rausher MD (1987) Components of conspecific host descrimination behavior in the butterfly Battus philenor. Ecology 68:245–253

    Article  Google Scholar 

  • Perugini M, Manera M, Grotta L et al (2011) Heavy metal (Hg, Cr, Cd, and Pb) contamination in urban areas and wildlife reserves: honeybees as bioindicators. Biol Trace Elem Res 140:170–176

    Article  CAS  PubMed  Google Scholar 

  • Pocock SJ, Smith M, Baghurst P (1994) Environmental lead and children’s intelligence: a systematic review of the epidemiological evidence. Br Med J 309:1189–1197

    Article  CAS  Google Scholar 

  • Posthuma L, Verweij RA, Widianarko B, Zonneveld C (1993) Life-history patterns in metal-adapted Collembola. Oikos 67:235–249

    Article  Google Scholar 

  • Rader R, Bartomeus I, Garibaldi LA et al (2016) Non-bee insects are important contributors to global crop pollination. Proc Natl Acad Sci 113:146–151

    Article  CAS  PubMed  Google Scholar 

  • Raine NE, Chittka L (2008) The correlation of learning speed and natural foraging success in bumble-bees. Proc R Soc Lond B Biol Sci 275:803–808

    Article  Google Scholar 

  • Rutowski RL (2000) Variation of eye size in butterflies: inter-and intraspecific patterns. J Zool 252:187–195

    Article  Google Scholar 

  • Rutowski RL (2003) Visual ecology of adult butterflies. In: Boggs CL, Watt WB, Ehrlich PR (eds) Butterflies ecology and evolution taking flight. The University of Chicago Press, Chicago, IL

  • Rutowski RL, McCoy L, Demlong MJ (2001) Visual mate detection in a territorial male butterfly (Asterocampa leilia): effects of distance and perch location. Behaviour 138:31–43

    Article  Google Scholar 

  • Ruuskanen S, Eeva T, Kotitalo P et al (2015) No delayed behavioral and phenotypic responses to experimental early-life lead exposure in great tits (Parus major). Environ Sci Pollut Res 22:2610–2621

    Article  CAS  Google Scholar 

  • Schmidt GH, Ibrahim NMM (1994) Heavy metal content (Hg2+, Cd2+, Pb2+) in various body parts: its impact on cholinesterase activity and binding glycoproteins in the grasshopper Aiolopus thalassinus adults. Ecotoxicol Environ Saf 29:148–164. doi:10.1016/0147-6513(94)90016-7

    Article  CAS  PubMed  Google Scholar 

  • Schwarz K, Pickett ST, Lathrop RG et al (2012) The effects of the urban built environment on the spatial distribution of lead in residential soils. Environ Pollut 163:32–39

    Article  CAS  PubMed  Google Scholar 

  • Sivinski J (1989) Mushroom body development in nymphalid butterflies: a correlate of learning? J Insect Behav 2:277–283

    Article  Google Scholar 

  • Snell-Rood EC, Papaj DR (2006) Learning signals within sensory environments: does host cue learning in butterflies depend on background? Anim Biol 56:173–192

    Article  Google Scholar 

  • Snell-Rood EC, Papaj DR (2009) Patterns of phenotypic plasticity in common and rare environments: a study of host use and color learning in the cabbage white butterfly Pieris rapae. Am Nat 173:615–631

    Article  PubMed  Google Scholar 

  • Snell-Rood EC, Papaj DR, Gronenberg W (2009) Brain size: a global or induced cost of learning? Brain Behav Evol 73:111–128

    Article  PubMed  Google Scholar 

  • Snell-Rood EC, Espeset A, Boser CJ et al (2014) Anthropogenic changes in sodium affect neural and muscle development in butterflies. Proc Natl Acad Sci 111:10221–10226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stewart WF, Schwartz BS (2007) Effects of lead on the adult brain: a 15-year exploration. Am J Ind Med 50:729–739

    Article  CAS  PubMed  Google Scholar 

  • Stewart WF, Schwartz BS, Davatzikos C et al (2006) Past adult lead exposure is linked to neurodegeneration measured by brain MRI. Neurology 66:1476–1484

    Article  CAS  PubMed  Google Scholar 

  • Tollett VD, Benvenutti EL, Deer LA, Rice TM (2009) Differential toxicity to Cd, Pb, and Cu in dragonfly larvae (Insecta: Odonata). Arch Environ Contam Toxicol 56:77–84

    Article  CAS  PubMed  Google Scholar 

  • Troetschler RG, Malone CM, Bucago ER, Johnston MR (1985) System for rearing Pieris rapae (Lepidoptera: Pieridae) on a noncruciferous artificial diet developed for Manduca sexta (Lepidoptera: Sphingidae). J Econ Entomol 78:1521–1523

    Article  Google Scholar 

  • Weiss MR (1995) Associative colour learning in a nymphalid butterfly. Ecol Entomol 20:298–301

    Article  Google Scholar 

  • Weiss MR (1997) Innate colour preferences and flexible colour learning in the pipevine swallowtail. Anim Behav 53:1043–1052

    Article  Google Scholar 

  • Weiss MR, Papaj DR (2003) Colour learning in two behavioural contexts: how much can a butterfly keep in mind? Anim Behav 65:425–434

    Article  Google Scholar 

  • Wittig R, Becker U (2010) The spontaneous flora around street trees in cities: a striking example for the worldwide homogenization of the flora of urban habitats. Flora-Morphol Distrib Funct Ecol Plants 205:704–709. doi:10.1016/j.flora.2009.09.001

    Google Scholar 

  • Worden BD, Papaj DR (2005) Flower choice copying in bumblebees. Biol Lett 1:504–507

    Article  PubMed  PubMed Central  Google Scholar 

  • Worden BD, Skemp AK, Papaj DR (2005) Learning in two contexts: the effects of interference and body size in bumblebees. J Exp Biol 208:2045–2053

    Article  PubMed  Google Scholar 

  • Xian X (1989) Effect of chemical forms of cadmium, zinc, and lead in polluted soils on their uptake by cabbage plants. Plant Soil 113:257–264. doi:10.1007/BF02280189

    Article  CAS  Google Scholar 

  • Zhang Y, Lambiase S, Fasola M et al (2001) Mortality and tissue damage by heavy metal contamination in the German cockroach, Blattella germanica (Blattaria, Blattellidae). Ital J Zool 68:137–145

    Article  CAS  Google Scholar 

  • Zhang Y-F, van Loon JJA, Wang C-Z (2010) Tarsal taste neuron activity and proboscis extension reflex in response to sugars and amino acids in Helicoverpa armigera (Hübner). J Exp Biol 213:2889–2895. doi:10.1242/jeb.042705

    Article  CAS  PubMed  Google Scholar 

  • Zhong Z, Zhang C, Rizak JD et al (2010) Chronic prenatal lead exposure impairs long-term memory in day old chicks. Neurosci Lett 476:23–26

    Article  CAS  PubMed  Google Scholar 

  • Ziemba KS, Rutowski RL (2000) Sexual dimorphism in eye morphology in a butterfly (Asterocampa leilia; Lepidoptera, Nymphalidae). Psyche (Stuttg) 103:25–36

    Article  Google Scholar 

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Acknowledgments

The authors would like to thank Meredith Steck for input on the experimental design and Eli Swanson and Sarah Jaumann for commenting on the manuscript. Input from two anonymous reviewers substantially improved this work. This study was funded by a University of Minnesota Undergraduate Research Opportunities Program Grant to KHP; the Snell-Rood lab was supported in part through NSF IOS-1354737.

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Correspondence to Emilie C. Snell-Rood.

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Data are accessible in DRYAD accession doi:10.5061/dryad.7f55p.

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This article is part of the Special Issue Animal cognition in a human dominated world.

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Philips, K.H., Kobiela, M.E. & Snell-Rood, E.C. Developmental lead exposure has mixed effects on butterfly cognitive processes. Anim Cogn 20, 87–96 (2017). https://doi.org/10.1007/s10071-016-1029-7

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