Exposure to sublethal concentrations of a pesticide or predator cues induces changes in brain architecture in larval amphibians
详细信息    查看全文
  • 作者:Sarah K. Woodley ; Brian M. Mattes ; Erika K. Yates ; Rick A. Relyea
  • 关键词:Insecticide ; Predator ; Brain plasticity ; Brain shape ; Metamorphosis ; Lithobates pipiens
  • 刊名:Oecologia
  • 出版年:2015
  • 出版时间:November 2015
  • 年:2015
  • 卷:179
  • 期:3
  • 页码:655-665
  • 全文大小:617 KB
  • 参考文献:Anderson BJ (2011) Plasticity of gray matter volume: the cellular and synaptic plasticity that underlies volumetric change. Dev Psychobiol 53:456–465CrossRef PubMed
    Barron MG, Woodburn K (1995) Ecotoxicology of chlorpyrifos. Rev Environ Contam Toxicol 144:1–93CrossRef PubMed
    Beck CW, Congdon JD (1999) Effects of individual variation in age and size at metamorphosis on growth and survivorship of southern toad (Bufo terrestris) metamorphs. Can J Zool 77:944–951CrossRef
    Berkowitz GS et al (2004) In utero pesticide exposure, maternal paraoxonase activity, and head circumference. Environ Health Perspect 112:388–391PubMedCentral CrossRef PubMed
    Bernabo I, Sperone E, Tripepi S, Brunelli E (2011) Toxicity of chlorpyrifos to larval Rana dalmatina: acute and chronic effects on survival, development, growth and gill apparatus. Arch Environ Contam Toxicol 61:704–718CrossRef PubMed
    Bock J, Rether K, Groger N, Xie L, Braun K (2014) Perinatal programming of emotional brain circuits: an integrative view from systems to molecules. Front Neurosci 8:11PubMedCentral CrossRef PubMed
    Boone MD (2005) Juvenile frogs compensate for small metamorph size with terrestrial growth: overcoming the effects of larval density and insecticide exposure. J Herp 39:416–423CrossRef
    Buchanan KL, Grindstaff JL, Pravosudov VV (2013) Condition dependence, developmental plasticity, and cognition: implications for ecology and evolution. Trends Ecol Evol 28:290–296PubMedCentral CrossRef PubMed
    Burns J, Rodd F (2008) Hastiness, brain size and predation regime affect ther performance of wild guppies in a spatial memory task. Anim Behav 76:911–922CrossRef
    Colborn T (2006) A case for revisiting the safety of pesticides: a closer look at neurodevelopment. Environ Health Perspect 114:10–17PubMedCentral CrossRef PubMed
    Cotman CW, Berchtold NC (2002) Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci 25:295–301CrossRef PubMed
    Crispo E, Chapman LJ (2010) Geographic variation in phenotypic plasticity in response to dissolved oxygen in an African cichlid fish. J Evol Biol 23:2091–2103CrossRef PubMed
    DeWitt T, Scheiner S (eds) (2004) Phenotypic plasticity: functional and conceptual approaches. Oxford University Press, Oxford
    Distal CA, Boone MD (2009) Effects of aquatic exposure to the insecticide carbaryl and density on aquatic and terrestrial growth and survival in American toads. Environ Toxic Chem 28:1963–1969CrossRef
    Emery PW (2005) Metabolic changes in malnutrition. Eye (Lond) 19:1029–1034CrossRef
    EPA (2006) Reregistration eligibility for chlorpyrifos. http://​www.​epagov/​pesticides/​reregistration/​status_​page_​chtm . Accessed 8 July 2015
    Frye CA et al (2012) Endocrine disrupters: a review of some sources, effects, and mechanisms of actions on behaviour and neuroendocrine systems. J Neuroendocrinol 24:144–159PubMedCentral CrossRef PubMed
    Gilbert S (2001) Ecological developmental biology: developmental biology meets the real world. Dev Biol 233:1–12CrossRef PubMed
    Gilbert S, Epel D (2009) Ecological developmental biology. Sinauer Associates, Sunderland
    Gonda A, Trokovic N, Herczeg G, Laurila A, Merila J (2010) Predation- and competition-mediated brain plasticity in Rana temporaria tadpoles. J Evol Biol 23:2300–2308
    Gonda A, Valimaki K, Herczeg G, Merila J (2012) Brain development and predation: plastic responses depend on evolutionary history. Biol Lett 8:249–252PubMedCentral CrossRef PubMed
    Gosner K (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190
    Hoverman JT, Cothran RD, Relyea R (2014) Generalist versus specialist strategies of plasticity: snail responses to predators that have different foraging modes. Freshw Biol 59:1101–1112CrossRef
    Hua J, Relyea R (2014) Chemical cocktails in aquatic systems: pesticide effects on the response and recovery of >20 animal taxa. Environ Pollut 189:18–26CrossRef PubMed
    Kaslin J, Ganz J, Brand M (2008) Proliferation, neurogenesis and regeneration in the non-mammalian vertebrate brain. Philos Trans R Soc Lond B Biol Sci 363:101–122PubMedCentral CrossRef PubMed
    Kihslinger RL, Nevitt GA (2006) Early rearing environment impacts cerebellar growth in juvenile salmon. J Exp Biol 209:504–509CrossRef PubMed
    Kollros J (1981) Transitions in the nervous system during amphibian metamorphosis. In: Gilbert LI, Frieden E (eds) Metamorphosis, a problem in developmental biology, 2nd edn. Plenum, New York, pp 445–459
    Kotrschal A et al (2013) Artificial selection on relative brain size in the guppy reveals costs and benefits of evolving a larger brain. Curr Biol 23:168–171PubMedCentral CrossRef PubMed
    Laurila A, Jarvi-Laturi M, Pakkasmaa S, Merila J (2004) Temporal variation in predation risk: stage-dependency, graded responses and fitness costs in tadpole antipredator defences. Oikos 107:90–99CrossRef
    Lima SL (1998) Nonlethal effects in the ecology of predator–prey interactions. Bioscience 48:25–34CrossRef
    Marco EM, Macri S, Laviola G (2011) Critical age windows for neurodevelopmental psychiatric disorders: evidence from animal models. Neurotox Res 19:286–307CrossRef PubMed
    Mazanti LE et al (2003) Aqueous-phase disappearance of atraxine, metolachlor, and chlorpyrifos in laboratory aquaria and outdoor macrocosms. Arch Environ Contam Toxicol 44:67–76CrossRef PubMed
    McCollum SA, Van Buskirk J (1996) Costs and benefits of a predator induced polyphenism in the gray treefrog Hyla chrysoscelis. Evolution 50:583–593CrossRef
    Pigliucci M (2001) Phenotypic plasticity: beyond nature and nurture. Johns Hopkins University Press, Baltimore
    Raucci F et al (2006) Proliferative activity in the frog brain: a PCNA-immunohistochemistry analysis. J Chem Neuroanat 32:127–142CrossRef PubMed
    Rauh VA et al (2012) Brain anomalies in children exposed prenatally to a common organophosphate pesticide. Proc Natl Acad Sci USA 109:7871–7876
    Relyea R (2002) The many faces of predation: how selection, induction, and thinning combine to alter prey phenotypes. Ecology 83:1953–1964CrossRef
    Relyea RA (2010) Multiple stressors and indirect food web effects of contaminants on herptofauna. In: Sparling DW, Linder G, Bishop CA, Krest SK (eds) Ecotoxicology of amphibians and reptiles, 2nd edn. CRC, Boca Raton, pp 475–485
    Relyea RA (2012) New effects of Roundup on amphibians: predators reduce herbicide mortality; herbicides induce antipredator morphology. Ecol Appl 22:634–647CrossRef PubMed
    Relyea RA, Auld JR (2005) Predator-and competitor-induced plasticity: how changes in foraging morphology affect phenotypic trade-offs. Ecology 86:1723–1729CrossRef
    Relyea RA, Werner EE (2000) Morphological plasticity in four larval anurans distributed along an environmental gradient. Copeia 2000:178–190CrossRef
    Richards SM, Kendall RJ (2002) Biochemical effects of chlorpyrifos on two developmental stages of Xenopus laevis. Environ Toxicol Chem 21:1826–1835CrossRef PubMed
    Richards SM, Kendall RJ (2003) Physical effects of chlorpyrifos on two stages of Xenopus laevis. J Toxicol Environ Health A 66:75–91CrossRef PubMed
    Rosenzweig MR, Bennett EL (1996) Psychobiology of plasticity: effects of training and experience on brain and behavior. Behav Brain Res 78:57–65CrossRef PubMed
    Roy TS, Seidler FJ, Slotkin TA (2004) Morphologic effects of subtoxic neonatal chlorpyrifos exposure in developing rat brain: regionally selective alterations in neurons and glia. Brain Res Dev Brain Res 148:197–206CrossRef PubMed
    Roy TS, Sharma V, Seidler FJ, Slotkin TA (2005) Quantitative morphological assessment reveals neuronal and glial deficits in hippocampus after a brief subtoxic exposure to chlorpyrifos in neonatal rats. Brain Res Dev Brain Res 155:71–80CrossRef PubMed
    Schlichting C, Pigliucci M (1998) Phenotypic evolution: a reaction norm perspective. Sinauer Associates, Sunderland
    Schoepper NM, Relyea R (2009) Phenotypic plasticity in response to fine-grained environmental variation in predation. Funct Ecol 23:587–594CrossRef
    Schoeppner NM, Relyea RA (2005) Damage, digestion, and defence: the roles of alarm cues and kairomones for inducing prey defences. Ecol Lett 8:505–512CrossRef PubMed
    Semlitsch RD, Scott DE, Pechmann JHK (1988) Time and size at metamorphosis related to adult fitness in Ambystoma talpoideum. Ecology 69:184–192CrossRef
    Slotkin TA (2004) Cholinergic systems in brain development and disruption by neurotoxicants: nicotine, environmental tobacco smoke, organophosphates. Toxicol Appl Pharmacol 198:132–151CrossRef PubMed
    Smith DC (1987) Adult recruitment in chorus frogs: effects of size and date at metamorphosis. Ecology 68:344–350CrossRef
    Trokovic N, Gonda A, Herczeg G, Laurila A, Merila J (2011) Brain plasticity over the metamorphic boundary: carry-over effect of larval environment on froglet brain development. J Evol Biol 24:1380–1385CrossRef PubMed
    Van Buskirk J (2009) Natural variation in morphology of larval amphibians: phenotypic plasticity in nature? Ecol Monogr 79:681–705CrossRef
    Van Buskirk J, Relyea RA (1998) Selection for phenotypic plasticity in Rana sylvatica tadpoles. Biol J Linn Soc 65:301–328CrossRef
    Weis J, Smith G, Zhou T, Santiago-Bass C, Weis P (2001) Effects of contaminants on behavior: biochemical mechanisms and ecological consequences. Bioscience 51:209–217CrossRef
    Widder PD, Bidwell JR (2008) Tadpole size, cholinesterase activity, and swim speed in four frog species after exposure to sub-lethal concentrations of chlorpyrifos. Aquat Toxicol 88:9–18CrossRef PubMed
    Wullimann MF, Rink E, Vernier P, Schlosser G (2005) Secondary neurogenesis in the brain of the African clawed frog, Xenopus laevis, as revealed by PCNA, Delta-1, Neurogenin-related-1, and NeuroD expression. J Comp Neurol 489:387–402CrossRef PubMed
    Zupanc GK (2001) Adult neurogenesis and neuronal regeneration in the central nervous system of teleost fish. Brain Behav Evol 58:250–275CrossRef PubMed
  • 作者单位:Sarah K. Woodley (1)
    Brian M. Mattes (2)
    Erika K. Yates (3)
    Rick A. Relyea (2)

    1. Department of Biological Sciences, Duquesne University, Pittsburgh, PA, 15282, USA
    2. Department of Biological Sciences, Rensselaer Polytechnic Institute, Troy, NY, 12180, USA
    3. Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA, 15260, USA
  • 刊物类别:Biomedical and Life Sciences
  • 刊物主题:Life Sciences
    Ecology
    Plant Sciences
  • 出版者:Springer Berlin / Heidelberg
  • ISSN:1432-1939
文摘
Naturally occurring environmental factors shape developmental trajectories to produce variable phenotypes. Such developmental phenotypic plasticity can have important effects on fitness, and has been demonstrated for numerous behavioral and morphological traits. However, surprisingly few studies have examined developmental plasticity of the nervous system in response to naturally occurring environmental variation, despite accumulating evidence for neuroplasticity in a variety of organisms. Here, we asked whether the brain is developmentally plastic by exposing larval amphibians to natural and anthropogenic factors. Leopard frog tadpoles were exposed to predator cues, reduced food availability, or sublethal concentrations of the pesticide chlorpyrifos in semi-natural enclosures. Mass, growth, survival, activity, larval period, external morphology, brain mass, and brain morphology were measured in tadpoles and after metamorphosis. Tadpoles in the experimental treatments had lower masses than controls, although developmental rates and survival were similar. Tadpoles exposed to predator cues or a high dose of chlorpyrifos had altered body shapes compared to controls. In addition, brains from tadpoles exposed to predator cues or a low dose of chlorpyrifos were narrower and shorter in several dimensions compared to control tadpoles and tadpoles with low food availability. Interestingly, the changes in brain morphology present at the tadpole stage did not persist in the metamorphs. Our results show that brain morphology is a developmentally plastic trait that is responsive to ecologically relevant natural and anthropogenic factors. Whether these effects on brain morphology are linked to performance or fitness is unknown.

© 2004-2018 中国地质图书馆版权所有 京ICP备05064691号 京公网安备11010802017129号

地址:北京市海淀区学院路29号 邮编:100083

电话:办公室:(+86 10)66554848;文献借阅、咨询服务、科技查新:66554700