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Critical Windows in Animal Development: Interactions Between Environment, Phenotype, and Time

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Development and Environment

Abstract

Observable phenotypic traits of an animal are a result of the interaction between the genome and environment. Differences in phenotypic traits between individuals induced by the environment, an indicator of phenotypic plasticity, may have immediate and long-term consequences for individuals, populations, and species. During development, animals are often most responsive or susceptible to changes in their environment, and phenotypic plasticity can be particularly prevalent. It is increasingly apparent that the way in which the environment influences an animal’s physiology may differ not just across a species’ lifetime but also within a species’ ontogeny. Periods of development during which an animal may show greater likelihood of phenotypic changes are termed “critical windows” or “sensitive periods.” Across animal taxa, experiments utilize exposures to particular environmental, chemical, or pharmacological stressors at certain time points of development to detect and understand critical windows during development. This chapter examines the emergence of critical windows as an important physiological concept using examples from the literature that span model and non-model invertebrates and vertebrates exposed to a range of environmental conditions. This chapter also outlines considerations for the continued search for critical windows. Critical window experimental designs can range in complexity, and variables such as the timing of exposures, if a single or multiple doses of a stressor are used, and when endpoints are assessed should be considered. A continued focus on critical windows will no doubt contribute to our growing knowledge of the interaction between the environment and physiology during animal development.

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References

  • Ackerman RA, Rahn H (1981) In vivo O2 and water vapor permeability of the hen’s eggshell during early development. Respir Physiol 45(1):1–8

    Article  CAS  PubMed  Google Scholar 

  • Ali S, Champagne DL, Alia A, Richardson MK (2011) Large-scale analysis of acute ethanol exposure in zebrafish development: a critical time window and resilience. PLoS One 6(5):e20037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andersen SL (2003) Trajectories of brain development: point of vulnerability or window of opportunity? Neurosci Biobehav Rev 27(1):3–18

    Article  PubMed  Google Scholar 

  • Andersen L, Holbech H, Gessbo Å, Norrgren L, Petersen GI (2003) Effects of exposure to 17α-ethinylestradiol during early development on sexual differentiation and induction of vitellogenin in zebrafish (Danio rerio). Comp Biochem Physiol C Toxicol Pharmacol 134(3):365–374

    Article  PubMed  CAS  Google Scholar 

  • Andersen HS, Gambling L, Holtrop G, McArdle HJ (2006) Maternal iron deficiency identifies critical windows for growth and cardiovascular development in the rat postimplantation embryo. J Nutr 136(5):1171–1177

    Article  CAS  PubMed  Google Scholar 

  • Angilletta MJ, Steury TD, Sears MW (2004) Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle. Integr Comp Biol 44(6):498–509

    Article  PubMed  Google Scholar 

  • Ankley GT, Johnson RD (2004) Small fish models for identifying and assessing the effects of endocrine-disrupting chemicals. ILAR J 45(4):469–483

    Article  CAS  PubMed  Google Scholar 

  • Aronzon CM, Sandoval MT, Herkovits J, Pérez-Coll CS (2011) Stage-dependent toxicity of 2,4-dichlorophenoxyacetic on the embryonic development of a South American toad, Rhinella arenarum. Environ Toxicol 26(4):373–381

    Article  CAS  PubMed  Google Scholar 

  • Bambang Y, Thuet P, Charmantier-Daures M, Trilles J-P, Charmantier G (1995) Effect of copper on survival and osmoregulation of various developmental stages of the shrimp Penaeus japonicus bate (Crustacea, Decapoda). Aquat Toxicol 33(2):125–139

    Article  CAS  Google Scholar 

  • Baroiller J, D’cotta H (2001) Environment and sex determination in farmed fish. Comp Biochem Physiol C Toxicol Pharmacol 130(4):399–409

    Article  CAS  PubMed  Google Scholar 

  • Barr M Jr, DeSesso JM, Lau CS, Osmond C, Ozanne SE, Sadler TW, Simmons RA, Sonawane BR (2000) Workshop to identify critical windows of exposure for children’s health: cardiovascular and endocrine work group summary. Environ Health Perspect 108(Suppl 3):569

    Article  PubMed  PubMed Central  Google Scholar 

  • Bavis RW (2005) Developmental plasticity of the hypoxic ventilatory response after perinatal hyperoxia and hypoxia. Respir Physiol Neurobiol 149(1):287–299

    Article  CAS  PubMed  Google Scholar 

  • Bavis RW, Mitchell GS (2008) Long-term effects of the perinatal environment on respiratory control. J Appl Physiol 104(4):1220–1229

    Article  PubMed  Google Scholar 

  • Bavis RW, Fallon SC, Dmitrieff EF (2013) Chronic hyperoxia and the development of the carotid body. Respir Physiol Neurobiol 185(1):94–104

    Article  CAS  PubMed  Google Scholar 

  • Beattie J, Pascoe D (1978) Cadmium uptake by rainbow trout, Salmo gairdneri eggs and alevins. J Fish Biol 13(5):631–637

    Article  CAS  Google Scholar 

  • Blaxter J (1969) Development: eggs and larvae. In: Hoar WS, Randall DJ (eds) Fish physiology, vol 3. Academic Press, San Diego, pp 177–252

    Google Scholar 

  • Boone MD, Hammond SA, Veldhoen N, Youngquist M, Helbing CC (2013) Specific time of exposure during tadpole development influences biological effects of the insecticide carbaryl in green frogs (Lithobates clamitans). Aquat Toxicol 130:139–148

    Article  PubMed  CAS  Google Scholar 

  • Bridges C (2000) Long-term effects of pesticide exposure at various life stages of the southern leopard frog (Rana sphenocephala). Arch Environ Con Tox 39(1):91–96

    Article  CAS  Google Scholar 

  • Bull J, Vogt R (1981) Temperature-sensitive periods of sex determination in emydid turtles. J Exp Zool 218(3):435–440

    Article  CAS  PubMed  Google Scholar 

  • Bunn T, Parsons P, Kao E, Dietert R (2001) Exposure to lead during critical windows of embryonic development: differential immunotoxic outcome based on stage of exposure and gender. Toxicol Sci 64(1):57–66

    Article  CAS  PubMed  Google Scholar 

  • Burggren WW (2014) Epigenetics as a source of variation in comparative animal physiology—or—Lamarck is lookin’ pretty good these days. J Exp Biol 217(5):682–689

    Article  PubMed  Google Scholar 

  • Burggren WW, Crews D (2014) Epigenetics in comparative biology: why we should pay attention. Integr Comp Biol 54(1):7–20

    Article  PubMed  PubMed Central  Google Scholar 

  • Burggren WW, Mueller CA (2015) Developmental critical windows and sensitive periods as 3-D constructs in time and space. Physiol Biochem Zool 88:91–102

    Article  PubMed  Google Scholar 

  • Burggren WW, Reyna KS (2011) Developmental trajectories, critical windows and phenotypic alteration during cardio-respiratory development. Respir Physiol Neurobiol 178:13–21

    Article  PubMed  Google Scholar 

  • Carvalho GR, Hughes RN (1983) The effect of food availability, female culture-density and photoperiod on ephippia production in Daphnia magna Straus (Crustacea: Cladocera). Freshwater Biol 13(1):37–46

    Article  Google Scholar 

  • Chan T, Burggren W (2005) Hypoxic incubation creates differential morphological effects during specific developmental critical windows in the embryo of the chicken (Gallus gallus). Respir Physiol Neurobiol 145(2–3):251–263

    Article  PubMed  Google Scholar 

  • Charmantier G, Charmantier-Daures M, Bouaricha N, Thuet P, Trilles J-P, Aiken D (1988) Ontogeny of osmoregulation and salinity tolerance in two decapod crustaceans: Homarus americanus and Penaeus japonicus. Biol Bull 175(1):102–110

    Article  Google Scholar 

  • Chiasson M, Benfey TJ, Martin-Robichaud DJ (2008) Gonadal differentiation in Atlantic cod, Gadus morhua L., and haddock, Melanogrammus aeglefinus (L.) Acta Ichtyol Piscat 38(2):127–133

    Article  Google Scholar 

  • Clarren SK, Astley SJ, Gunderson VM, Spellman D (1992) Cognitive and behavioral deficits in nonhuman primates associated with very early embryonic binge exposures to ethanol. J Pediatr 121(5):789–796

    Article  CAS  PubMed  Google Scholar 

  • Colombo J (1982) The critical period concept: research, methodology, and theoretical issues. Psychol Bull 91(2):260

    Article  CAS  PubMed  Google Scholar 

  • Conover DO (1984) Adaptive significance of temperature-dependent sex determination in a fish. Am Nat 123:297–313

    Article  Google Scholar 

  • Conover DO, Fleisher MH (1986) Temperature-sensitive period of sex determination in the Atlantic silverside, Menidia menidia. Can J Fish Aquat Sci 43(3):514–520

    Article  Google Scholar 

  • Conte FP (1984) Structure and function of the crustacean larval salt gland. Int Rev Cytol 91:45–106

    Article  CAS  Google Scholar 

  • Copeland J, Dzialowski EM (2009) Effects of hypoxic and hyperoxic incubation on the reactivity of the chicken embryo (Gallus gallus) ductus arteriosi in response to catecholamines and oxygen. Exp Physiol 94(1):152–161

    Article  CAS  PubMed  Google Scholar 

  • Croghan P (1958) The mechanism of osmotic regulation in Artemia salina (L.): the physiology of the branchiae. J Exp Biol 35(1):234–242

    Article  CAS  Google Scholar 

  • Cronise K, Marino MD, Tran TD, Kelly SJ (2001) Critical periods for the effects of alcohol exposure on learning in rats. Behav Neurosci 115(1):138

    Article  CAS  PubMed  Google Scholar 

  • Crossley DA II, Altimiras J (2005) Cardiovascular development in embryos of the American alligator Alligator mississippiensis: effects of chronic and acute hypoxia. J Exp Biol 208(Pt 1):31–39

    Article  Google Scholar 

  • Crossley DA II, Burggren WW, Altimiras J (2003) Cardiovascular regulation during hypoxia in embryos of the domestic chicken Gallus gallus. Am J Physiol Regul Integr Comp Physiol 284(1):R219–R226

    Article  CAS  PubMed  Google Scholar 

  • DeCoursey PJ, Vernberg WB (1972) Effect of mercury on survival, metabolism and behaviour of larval Uca pugilator (Brachyura). Oikos 23:241–247

    Article  CAS  Google Scholar 

  • Deeming D, Ferguson M, Mittwoch U, Wolf U, Dorizzi M, Zaborski P, Sharma H (1988) Environmental regulation of sex determination in reptiles. Philos T Roy Soc B 322(1208):19–39

    CAS  Google Scholar 

  • Degitz SJ, Kosian PA, Makynen EA, Jensen KM, Ankley GT (2000) Stage-and species-specific developmental toxicity of all-trans retinoic acid in four native North American ranids and Xenopus laevis. Toxicol Sci 57(2):264–274

    Article  CAS  PubMed  Google Scholar 

  • Dietert RR, Etzel RA, Chen D, Halonen M, Holladay SD, Jarabek AM, Landreth K, Peden DB, Pinkerton K, Smialowicz RJ (2000) Workshop to identify critical windows of exposure for children’s health: immune and respiratory systems work group summary. Environ Health Perspect 108(Suppl 3):483

    Article  PubMed  PubMed Central  Google Scholar 

  • Dietert R, Lee J, Bunn T (2002) Developmental immunotoxicology: emerging issues. Hum Exp Toxicol 21(9–10):479–485

    Article  CAS  PubMed  Google Scholar 

  • Doyle JE, McMahon BR (1995) Effects of acid exposure in the brine shrimp Artemia franciscana during development in seawater. Comp Biochem Physiol A 112:123–129

    Article  Google Scholar 

  • Dzialowski EM, von Plettenberg D, Elmonoufy NA, Burggren WW (2002) Chronic hypoxia alters the physiological and morphological trajectories of developing chicken embryos. Comp Biochem Physiol A 131(4):713–724

    Article  Google Scholar 

  • Eme J, Altimiras J, Hicks JW, Crossley DA II (2011a) Hypoxic alligator embryos: chronic hypoxia, catecholamine levels and autonomic responses of in ovo alligators. Comp Biochem Physiol A 160(3):412–420

    Article  CAS  Google Scholar 

  • Eme J, Hicks JW, Crossley DA II (2011b) Chronic hypoxic incubation blunts a cardiovascular reflex loop in embryonic American alligator (Alligator mississippiensis). J Comp Physiol B 181(7):981–990

    Article  CAS  PubMed  Google Scholar 

  • Eme J, Rhen T, Tate K, Gruchalla K, Kohl Z, Slay C, Crossley D II (2013) Plasticity of cardiovascular function in snapping turtle embryos (Chelydra serpentina): chronic hypoxia alters autonomic regulation and gene expression. Am J Physiol Regul Integr Comp Physiol 304:R966–R979

    Article  CAS  PubMed  Google Scholar 

  • Eme J, Rhen T, Crossley DA II (2014) Adjustments in cholinergic, adrenergic and purinergic control of cardiovascular function in snapping turtle embryos (Chelydra serpentina) incubated in chronic hypoxia. J Comp Physiol B 184(7):891–902

    Article  CAS  PubMed  Google Scholar 

  • Eme J, Mueller CA, Manzon RG, Somers CM, Boreham DR, Wilson JY (2015) Critical windows in embryonic development: shifting incubation temperatures alter heart rate and oxygen consumption of Lake whitefish (Coregonus clupeaformis) embryos and hatchlings. Comp Biochem Physiol A 179:71–80

    Article  CAS  Google Scholar 

  • Emlen DJ, Nijhout HF (1999) Hormonal control of male horn length dimorphism in the dung beetle Onthophagus taurus (Coleoptera: Scarabaeidae). J Insect Physiol 45(1):45–53

    Article  CAS  PubMed  Google Scholar 

  • Emlen D, Nijhout H (2001) Hormonal control of male horn length dimorphism in Onthophagus taurus (Coleoptera: Scarabaeidae): a second critical period of sensitivity to juvenile hormone. J Insect Physiol 47(9):1045–1054

    Article  CAS  PubMed  Google Scholar 

  • Feder ME (1985) Thermal acclimation of oxygen consumption and cardiorespiratory frequencies in frog larvae. Physiol Zool 58(3):303–311

    Article  Google Scholar 

  • Feist G, Schreck CB, Fitzpatrick MS, Redding JM (1990) Sex steroid profiles of coho salmon (Oncorhynchus kisutch) during early development and sexual differentiation. Gen Comp Endocrinol 80(2):299–313

    Article  CAS  PubMed  Google Scholar 

  • Fent K, Meier W (1994) Effects of triphenyltin on fish early life stages. Arch Environ Con Tox 27(2):224–231

    Article  CAS  Google Scholar 

  • Ferguson MW, Joanen T (1982) Temperature of egg incubation determines sex in Alligator mississippiensis. Nature 296:850–853

    Article  CAS  PubMed  Google Scholar 

  • Ferner K, Mortola JP (2009) Ventilatory response to hypoxia in chicken hatchlings: a developmental window of sensitivity to embryonic hypoxia. Respir Physiol Neurobiol 165(1):49–53

    Article  PubMed  Google Scholar 

  • Finstad AG, Jonsson B (2012) Effect of incubation temperature on growth performance in Atlantic salmon. Mar Ecol-Prog Ser 454:75–82

    Article  Google Scholar 

  • Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL (2001) Effects of size and temperature on metabolic rate. Science 293(5538):2248–2251

    Article  CAS  PubMed  Google Scholar 

  • Gimeno S, Komen H, Venderbosch PW, Bowmer T (1997) Disruption of sexual differentiation in genetic male common carp (Cyprinus carpio) exposed to an alkylphenol during different life stages. Environ Sci Technol 31(10):2884–2890

    Article  CAS  Google Scholar 

  • Glas PS, Courtney LA, Rayburn JR, Fisher WS (1997) Embryonic coat of the grass shrimp Palaemonetes pugio. Biol Bull 192(2):231–242

    Article  CAS  PubMed  Google Scholar 

  • González-Doncel M, Fernández-Torija C, Hinton D, Tarazona J (2004) Stage-specific toxicity of cypermethrin to medaka (Oryzias latipes) eggs and embryos using a refined methodology for an in vitro fertilization bioassay. Arch Environ Con Tox 48(1):87–98

    Article  CAS  Google Scholar 

  • Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190

    Google Scholar 

  • Grabowski CT, Paar JA (1958) The teratogenic effects of graded doses of hypoxia on the chick embryo. Am J Anat 103(3):313–347

    Article  CAS  PubMed  Google Scholar 

  • Green DW, Williams KA, Pascoe D (1986) The acute and chronic toxicity of cadmium to different life history stages of the freshwater crustacean Asellus aquaticus (L). Arch Environ Con Tox 15(5):465–471

    Article  CAS  Google Scholar 

  • Greulich K, Pflugmacher S (2003) Differences in susceptibility of various life stages of amphibians to pesticide exposure. Aquat Toxicol 65(3):329–336

    Article  CAS  PubMed  Google Scholar 

  • Hackmann E, Reinboth R (1974) Delimitation of the critical stage of hormone-influenced sex differentiation in Hemihaplochromis multicolor (Hilgendorf)(Cichlidae). Gen Comp Endocrinol 22(1):42–53

    Article  CAS  PubMed  Google Scholar 

  • Hakeem GF, Oddy L, Holcroft CA, Abenhaim HA (2015) Incidence and determinants of sudden infant death syndrome: a population-based study on 37 million births. World J Pediatr 11:41–47

    Article  PubMed  Google Scholar 

  • Hanlon SM, Parris MJ (2014) The interactive effects of chytrid fungus, pesticides, and exposure timing on gray treefrog (Hyla versicolor) larvae. Environ Toxicol Chem 33(1):216–222

    Article  CAS  PubMed  Google Scholar 

  • Hanlon SM, Kerby JL, Parris MJ (2012) Unlikely remedy: fungicide clears infection from pathogenic fungus in larval southern leopard frogs (Lithobates sphenocephalus). PLoS One 7(8):e43573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harrington RW (1968) Delimitation of the thermolabile phenocritical period of sex determination and differentiation in the ontogeny of the normally hermaphroditic fish Rivulus marmoratus Poey. Physiol Zool 41:447–460

    Article  Google Scholar 

  • Hayes TB (1997) Steroids as potential modulators of thyroid hormone activity in anuran metamorphosis. Am Zool 37(2):185–194

    Article  CAS  Google Scholar 

  • Hendry C, Martin-Robichaud D, Benfey T (2002) Gonadal sex differentiation in Atlantic halibut. J Fish Biol 60(6):1431–1442

    Article  Google Scholar 

  • Hensch TK (2004) Critical period regulation. Annu Rev Neurosci 27(1):549–579

    Article  CAS  PubMed  Google Scholar 

  • Herzig A, Winkler H (1986) The influence of temperature on the embryonic development of three cyprinid fishes, Abramis brama, Chalcalburnus chalcoides mento and Vimba vimba. J Fish Biol 28:171–181

    Article  Google Scholar 

  • Hill RL Jr, Janz DM (2003) Developmental estrogenic exposure in zebrafish (Danio rerio): I. Effects on sex ratio and breeding success. Aquat Toxicol 63(4):417–429

    Article  CAS  PubMed  Google Scholar 

  • Hillman R (1977) Polygenic control of Drosophila morphogenesis during the stages of determination and specification of adult structures. Am Zool 17(3):521–533

    Article  Google Scholar 

  • Ho DH, Burggren WW (2010) Epigenetics and transgenerational transfer: a physiological perspective. J Exp Biol 213(1):3–16

    Article  CAS  PubMed  Google Scholar 

  • Hogan NS, Duarte P, Wade MG, Lean DRS, Trudeau VL (2008) Estrogenic exposure affects metamorphosis and alters sex ratios in the northern leopard frog (Rana pipiens): identifying critically vulnerable periods of development. Gen Comp Endocrinol 156(3):515–523

    Article  CAS  PubMed  Google Scholar 

  • Hunt J, Simmons LW (1997) Patterns of fluctuating asymmetry in beetle horns: an experimental examination of the honest signalling hypothesis. Behav Ecol Sociobiol 41(2):109–114

    Article  Google Scholar 

  • Hunter GA, Donaldson EM (1983) Hormonal sex control and its application to fish culture. In: Hoar WS, Randall DJ, Donaldson EM (eds) Fish physiology, vol 9. Academic Press, New York, pp 223–303

    Google Scholar 

  • Itow T, Loveland R, Botton M (1998) Developmental abnormalities in horseshoe crab embryos caused by exposure to heavy metals. Arch Environ Con Tox 35(1):33–40

    Article  CAS  Google Scholar 

  • Iwamatsu T (2004) Stages of normal development in the medaka Oryzias latipes. Mech Develop 121(7):605–618

    Article  CAS  Google Scholar 

  • Johnson JS, Newport EL (1989) Critical period effects in second language learning: the influence of maturational state on the acquisition of English as a second language. Cogn Psychol 21:60–99

    Article  CAS  PubMed  Google Scholar 

  • Johnson PT, Kellermanns E, Bowerman J (2011) Critical windows of disease risk: amphibian pathology driven by developmental changes in host resistance and tolerance. Funct Ecol 25(3):726–734

    Article  Google Scholar 

  • Jones DK, Hammond JI, Relyea RA (2011) Competitive stress can make the herbicide roundup® more deadly to larval amphibians. Environ Toxicol Chem 30(2):446–454

    Article  CAS  PubMed  Google Scholar 

  • Kam YC (1993) Physiological effects of hypoxia on metabolism and growth of turtle embryos. Respir Physiol 92:127–138

    Article  CAS  PubMed  Google Scholar 

  • Kamler E, Keckeis H, Bauer-Nemeschkal E (1998) Temperature-induced changes of survival, development and yolk partitioning in Chondrostoma nasus. J Fish Biol 53:658–682

    Google Scholar 

  • Karraker NE, Arrigoni J, Dudgeon D (2010) Effects of increased salinity and an introduced predator on lowland amphibians in southern China: species identity matters. Biol Conserv 143(5):1079–1086

    Article  Google Scholar 

  • Kefford BJ, Papas PJ, Nugegoda D (2003) Relative salinity tolerance of macroinvertebrates from the Barwon River, Victoria, Australia. Mar Freshw Res 54(6):755–765

    Article  CAS  Google Scholar 

  • Kettlewell JR, Raymond CS, Zarkower D (2000) Temperature-dependent expression of turtle Dmrt 1 prior to sexual differentiation. Genesis 26(3):174–178

    Article  CAS  PubMed  Google Scholar 

  • Kikuyama S, Kawamura K, Tanaka S, Yamamoto K (1993) Aspects of amphibian metamorphosis: hormonal control. In: Jeon KW, Jarvik J (eds) International review of cytology, vol 145. Academic Press, San Diego, pp 105–105

    Google Scholar 

  • Knudsen E (2004) Sensitive periods in the development of the brain and behavior. J Cognitive Neurosci 16(8):1412–1425

    Article  Google Scholar 

  • Kochhar D, Penner JD, Tellone CI (1984) Comparative teratogenic activities of two retinoids: effects on palate and limb development. Teratogen Carcin Mut 4(4):377–387

    Article  CAS  Google Scholar 

  • Koger CS, Teh SJ, Hinton DE (2000) Determining the sensitive developmental stages of intersex induction in medaka (Oryzias latipes) exposed to 17β-estradiol or testosterone. Mar Environ Res 50(1–5):201–206

    Article  CAS  PubMed  Google Scholar 

  • Korpelainen H (1990) Sex ratios and conditions required for environmental sex determination in animals. Biol Rev 65(2):147–184

    Article  CAS  PubMed  Google Scholar 

  • Kuramoto M (1975) Adaptive significance in oxygen consumption of frog embryos in relation to the environmental temperatures. Comp Biochem Physiol A 52(1):59–62

    Article  CAS  PubMed  Google Scholar 

  • Landreth K (2002) Critical windows in development of the rodent immune system. Hum Exp Toxicol 21(9–10):493–498

    Article  CAS  PubMed  Google Scholar 

  • Latham KE, Just JJ (1989) Oxygen availability provides a signal for hatching in the rainbow trout (Salmo gairdneri) embryo. Can J Fish Aquat Sci 46:55–58

    Article  Google Scholar 

  • Lavolpe M, Greco LL, Kesselman D, Rodríguez E (2004) Differential toxicity of copper, zinc, and lead during the embryonic development of Chasmagnathus granulatus (Brachyura, Varunidae). Environ Toxicol Chem 23(4):960–967

    Article  CAS  PubMed  Google Scholar 

  • Lee J-E, Chen S, Golemboski KA, Parsons PJ, Dietert RR (2001) Developmental windows of differential lead-induced immunotoxicity in chickens. Toxicology 156(2):161–170

    Article  CAS  PubMed  Google Scholar 

  • Lin H-P, Thuet P, Trilles JP, Mounet-Guillaume R, Charmantier G (1993) Effects of ammonia on survival and osmoregulation of various development stages of the shrimp Penaeus japonicus. Mar Biol 117(4):591–598

    Article  CAS  Google Scholar 

  • Liu Q, Wong-Riley MT (2010) Postnatal changes in the expressions of serotonin 1A, 1B, and 2A receptors in ten brain stem nuclei of the rat: implication for a sensitive period. Neuroscience 165(1):61–78

    Article  CAS  PubMed  Google Scholar 

  • Liu Q, Lowry TF, Wong-Riley MT (2006) Postnatal changes in ventilation during normoxia and acute hypoxia in the rat: implication for a sensitive period. J Physiol 577(3):957–970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Q, Fehring C, Lowry TF, Wong-Riley MT (2009) Postnatal development of metabolic rate during normoxia and acute hypoxia in rats: implication for a sensitive period. J Appl Physiol 106(4):1212–1222

    Article  PubMed  Google Scholar 

  • López Greco L, Rodriguez E, Bolaños J, Hernandez G, Fingerman M (2002) Toxicity of copper sulphate during early and late embryonic development of a palaemonid shrimp (Crustacea). Invertebr Reprod Dev 41(1–3):165–170

    Article  Google Scholar 

  • Lumey L, Khalangot MD, Vaiserman AM (2015) Association between type 2 diabetes and prenatal exposure to the Ukraine famine of 1932–33: a retrospective cohort study. Lancet Diabetes Endocrinol 3(10):787–794

    Article  CAS  PubMed  Google Scholar 

  • Lusk LA, Wai KC, Moon-Grady AJ, Steurer MA, Keller RL (2015) Persistence of pulmonary hypertension by echocardiography predicts short-term outcomes in congenital diaphragmatic hernia. J Pediatr 166(2):251–256. e251

    Article  PubMed  Google Scholar 

  • Maack G, Segner H (2004) Life-stage-dependent sensitivity of zebrafish (Danio rerio) to estrogen exposure. Comp Biochem Physiol C Toxicol Pharmacol 139(1–3):47–55

    Article  PubMed  CAS  Google Scholar 

  • Macqueen DJ, Robb DH, Olsen T, Melstveit L, Paxton CG, Johnston IA (2008) Temperature until the ‘eyed stage’of embryogenesis programmes the growth trajectory and muscle phenotype of adult Atlantic salmon. Biol Lett 4:294–298

    Article  PubMed  PubMed Central  Google Scholar 

  • Mariño-Balsa J, Poza E, Vázquez E, Beiras R (2000) Comparative toxicity of dissolved metals to early larval stages of Palaemon serratus, Maja squinado, and Homarus gammarus (Crustacea: Decapoda). Arch Environ Con Tox 39(3):345–351

    Article  Google Scholar 

  • Mattson SN, Riley EP (1998) A review of the neurobehavioral deficits in children with fetal alcohol syndrome or prenatal exposure to alcohol. Alcohol Clin Exp Res 22(2):279–294

    Article  CAS  PubMed  Google Scholar 

  • McCutcheon IE, Metcalfe J, Metzenberg AB, Ettinger T (1982) Organ growth in hyperoxic and hypoxic chick embryos. Respir Physiol 50(2):153–163

    Article  CAS  PubMed  Google Scholar 

  • McLaren IA, Cooley JM (1972) Temperature adaptation of embryonic development rate among frogs. Physiol Zool 45:223–228

    Article  Google Scholar 

  • Meredith R (2015) Sensitive and critical periods during neurotypical and aberrant neurodevelopment: a framework for neurodevelopmental disorders. Neurosci Biobehav R 50:180–188

    Article  CAS  Google Scholar 

  • Mills NE, Barnhart MC (1999) Effects of hypoxia on embryonic development in two Ambystoma and two Rana species. Physiol Biochem Zool 72:179–188

    Article  CAS  PubMed  Google Scholar 

  • Mueller CA, Joss JMP, Seymour RS (2011a) Effects of environmental oxygen on development and respiration of Australian lungfish (Neoceratodus forsteri) embryos. J Comp Physiol B 181:941–952

    Article  CAS  PubMed  Google Scholar 

  • Mueller CA, Joss JMP, Seymour RS (2011b) The energy cost of embryonic development in fishes and amphibians, with emphasis on new data from the Australian lungfish, Neoceratodus forsteri. J Comp Physiol B 181:43–52

    Article  PubMed  Google Scholar 

  • Mueller CA, Eme J, Burggren WW, Rundle SD, Roghair RD (2015a) Challenges and opportunities in integrative developmental physiology. Comp Biochem Physiol A 184:113–124

    Article  CAS  Google Scholar 

  • Mueller CA, Eme J, Manzon RG, Somers CM, Boreham DR, Wilson JY (2015b) Embryonic critical windows: changes in incubation temperature alter survival, hatchling phenotype and cost of development in Lake whitefish (Coregonus clupeaformis). J Comp Physiol B 185:315–331

    Article  PubMed  Google Scholar 

  • Mueller CA, Willis E, Burggren WW (2016) Salt sensitivity of the morphometry of Artemia franciscana during development: a demonstration of 3D critical windows. J Exp Biol 219(4):571–581

    PubMed  Google Scholar 

  • Murdock C, Wibbels T (2002) Expression of Dmrt1 in a turtle with temperature-dependent sex determination. Cytogenet Genome Res 101(3–4):302–308

    Google Scholar 

  • Nakamura M, Takahashi H (1973) Gonadal sex differentiation in Tilapia mossambica, with special regard to the time of estrogen treatment effective in inducing complete feminization of genetic males. Bull Fac Fish Hokkaido Univ 24(1):1–13

    Google Scholar 

  • Olmstead AW, Leblanc GA (2002) Juvenoid hormone methyl farnesoate is a sex determinant in the crustacean Daphnia magna. J Exp Zool 293(7):736–739

    Article  CAS  PubMed  Google Scholar 

  • Oxendine SL, Cowden J, Hinton DE, Padilla S (2006) Vulnerable windows for developmental ethanol toxicity in the Japanese medaka fish (Oryzias latipes). Aquat Toxicol 80(4):396–404

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Coll C, Herkovits J (1990) Stage dependent susceptibility to lead in Bufo arenarum embryos. Environ Pollut 63(3):239–245

    Article  PubMed  Google Scholar 

  • Petranka JW, Just JJ, Crawford EC (1982) Hatching of amphibian embryos: the physiological trigger. Science 217:257–259

    Article  CAS  PubMed  Google Scholar 

  • Pieau C, Dorizzi M (1981) Determination of temperature sensitive stages for sexual differentiation of the gonads in embryos of the turtle, Emys orbicularis. J Morphol 170(3):373–382

    Article  PubMed  Google Scholar 

  • Piferrer F, Donaldson EM (1989) Gonadal differentiation in coho salmon, Oncorhynchus kisutch, after a single treatment with androgen or estrogen at different stages during ontogenesis. Aquaculture 77(2):251–262

    Article  Google Scholar 

  • Price JW (1934a) The embryology of the whitefish Coregonus Clupeaformis, (Mitchill). Part I. Ohio J Sci 34:287–305

    Google Scholar 

  • Price JW (1934b) The embryology of the whitefish Coregonus Clupeaformis, (Mitchill). Part II. Organogenesis. Ohio J Sci 34:399–414

    Google Scholar 

  • Price JW (1935) The embryology of the whitefish Coregonus Clupeaformis, (Mitchill). Part III. The second half of the incubation period. Ohio J Sci 35:40–53

    Google Scholar 

  • Pryor JL, Hughes C, Foster W, Hales BF, Robaire B (2000) Critical windows of exposure for children’s health: the reproductive system in animals and humans. Environ Health Perspect 108(Suppl 3):491

    Article  PubMed  PubMed Central  Google Scholar 

  • Reece EA, Wiznitzer A, Homko CJ, Hagay Z, Wu YK (1996) Synchronization of the factors critical for diabetic teratogenesis: an in vitro model. Am J Obstet Gynecol 174(4):1284–1288

    Article  CAS  PubMed  Google Scholar 

  • Relyea RA, Mills N (2001) Predator-induced stress makes the pesticide carbaryl more deadly to gray treefrog tadpoles (Hyla versicolor). P Natl Acad Sci USA 98(5):2491–2496

    Article  CAS  Google Scholar 

  • Rice D, Barone S Jr (2000) Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect 108(Suppl 3):511

    Article  PubMed  PubMed Central  Google Scholar 

  • Romanoff AL (1967) Biochemistry of the avian embryo. Wiley, New York

    Google Scholar 

  • Rombough PJ (1988) Respiratory gas exchange, aerobic metabolism, and effects of hypoxia during early life. In: Hoar WS, Randall DJ (eds) The physiology of developing fish, Fish physiology, vol 11. Academic Press, San Diego, pp 59–161

    Chapter  Google Scholar 

  • Rombough PJ (2003) Development rate: modelling developmental time and temperature. Nature 424(6946):268–269

    Article  CAS  PubMed  Google Scholar 

  • Sarre SD, Georges A, Quinn A (2004) The ends of a continuum: genetic and temperature-dependent sex determination in reptiles. BioEssays 26(6):639–645

    Article  PubMed  Google Scholar 

  • Schneider ML, Moore CF, Becker EF (2001) Timing of moderate alcohol exposure during pregnancy and neonatal outcome in rhesus monkeys (Macaca mulatta). Alcohol Clin Exp Res 25(8):1238–1245

    Article  CAS  PubMed  Google Scholar 

  • Schotthoefer A, Koehler A, Meteyer C, Cole R (2003) Influence of Ribeiroia infection on limb development and survival of northern leopard frogs: effects of host-stage and parasite exposure level. Can J Zool 81:1144–1153

    Article  Google Scholar 

  • Scott GR, Johnston IA (2012) Temperature during embryonic development has persistent effects on thermal acclimation capacity in zebrafish. P Natl Acad Sci USA 109(35):14247–14252

    Article  CAS  Google Scholar 

  • Selevan SG, Kimmel CA, Mendola P (2000) Identifying critical windows of exposure for children’s health. Environ Health Perspect 108(Suppl 3):451

    Article  PubMed  PubMed Central  Google Scholar 

  • Seymour RS, Roberts JD, Mitchell NJ, Blaylock AJ (2000) Influence of environmental oxygen on development and hatching of aquatic eggs of the Australian frog, Crinia georgiana. Physiol Biochem Zool 73:501–507

    Article  CAS  PubMed  Google Scholar 

  • Sive H, Draper B, Harland R, Weintraub H (1990) Identification of a retinoic acid-sensitive period during primary axis formation in Xenopus laevis. Genes Dev 4:932–942

    Article  CAS  PubMed  Google Scholar 

  • Sollid SA, Lorz HV, Stevens DG, Bartholomew JL (2003) Age-dependent susceptibility of Chinook salmon to Myxobolus cerebralis and effects of sustained parasite challenges. J Aquat Anim Health 15(2):136–146

    Article  Google Scholar 

  • Stross RG, Hill JC (1965) Diapause induction in Daphnia requires two stimuli. Science 150(3702):1462–1464

    Article  CAS  PubMed  Google Scholar 

  • Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, Waller RW (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306(5702):1783–1786

    Article  CAS  PubMed  Google Scholar 

  • Sulik KK, Dehart DB, Rogers JM, Chernoff N (1995) Teratogenicity of low doses of all-trans retinoic acid in presomite mouse embryos. Teratology 51(6):398–403

    Article  CAS  PubMed  Google Scholar 

  • Svitok P, Molcan L, Vesela A, Kruzliak P, Moravcik R, Zeman M (2015) Increased salt intake during early ontogenesis lead to development of arterial hypertension in salt-resistant Wistar rats. Clin Exp Hypertens 37(2):142–147

    Article  CAS  PubMed  Google Scholar 

  • Sweeney BW, Schnack JA (1977) Egg development, growth and metabolism of Sigara alternata (say) (Hemiptera: Corixidae) in fluctuating thermal environments. Ecology 58:265–277

    Article  Google Scholar 

  • Tate KB, Kohl ZF, Eme J, Rhen T, Crossley DA (2015) Critical windows of cardiovascular susceptibility to developmental hypoxia in common snapping turtle (Chelydra serpentina) embryos. Physiol Biochem Zool 88:103–115

    Article  PubMed  Google Scholar 

  • Taylor LW, Kreutziger GO (1965) The gaseous environment of the chick embryo in relation to its development and hatchability 2. Effect of carbon dioxide and oxygen levels during the period of the fifth through the eighth days of incubation. Poult Sci 44(1):98–106

    Article  CAS  PubMed  Google Scholar 

  • Taylor LW, Kreutziger GO (1966) The gaseous environment of the chick embryo in relation to its development and hatchability 3. Effect of carbon dioxide and oxygen levels during the period of the ninth through the twelfth days of incubation. Poult Sci 45(5):867–884

    Article  Google Scholar 

  • Taylor LW, Kreutziger GO (1969) The gaseous environment of the chick embryo in relation to its development and hatchability 4. Effect of carbon dioxide and oxygen levels during the period of the thirteenth through the sixteenth days of incubation. Poult Sci 48(3):871–877

    Article  CAS  PubMed  Google Scholar 

  • Taylor LW, Sjodin RA, Gunns C (1956) The gaseous environment of the chick embryo in relation to its development and hatchability 1. Effect of carbon dioxide and oxygen levels during the first four days of incubation upon hatchability. Poult Sci 35(6):1206–1215

    Article  CAS  Google Scholar 

  • Taylor LW, Kreutzige GO, Abercrombie GL (1971) The gaseous environment of the chick embryo in relation to its development and hatchability 5. Effect of carbon dioxide and oxygen levels during the terminal days of incubation. Poult Sci 50(1):66–78

    Article  CAS  PubMed  Google Scholar 

  • Tazawa H (1981) Effect of O2 and CO2 in N2, He, and SF6 on chick embryo blood pressure and heart rate. J Appl Physiol 51(4):1017–1022

    Article  CAS  PubMed  Google Scholar 

  • Tazawa H, Hashimoto Y, Nakazawa S, Whittow GC (1992) Metabolic responses of chicken embryos and hatchlings to altered O2 environments. Respir Physiol 88:37–50

    Article  CAS  PubMed  Google Scholar 

  • Tran TD, Cronise K, Marino MD, Jenkins WJ, Kelly SJ (2000) Critical periods for the effects of alcohol exposure on brain weight, body weight, activity and investigation. Behav Brain Res 116(1):99–110

    Article  CAS  PubMed  Google Scholar 

  • Turner BJ, Davis WP, Taylor D (1992) Abundant males in populations of a selfing hermaphrodite fish, Rivulus marmoratus, from some Belize cays. J Fish Biol 40(2):307–310

    Article  Google Scholar 

  • Tyler C, Jobling S, Sumpter J (1998) Endocrine disruption in wildlife: a critical review of the evidence. CRC Cr Rev Toxicol 28(4):319–361

    Article  CAS  Google Scholar 

  • Uylings HB (2006) Development of the human cortex and the concept of “critical” or “sensitive” periods. Lang Learn 56(s1):59–90

    Article  Google Scholar 

  • van Aerle R, Pounds N, Hutchinson TH, Maddix S, Tyler CR (2002) Window of sensitivity for the estrogenic effects of ethinylestradiol in early life-stages of fathead minnow, Pimephales promelas. Ecotoxicology 11(6):423–434

    Article  PubMed  Google Scholar 

  • Van Leeuwen C, Griffioen P, Vergouw W, Maas-Diepeveen J (1985) Differences in susceptibility of early life stages of rainbow trout (Salmo gairdneri) to environmental pollutants. Aquat Toxicol 7(1):59–78

    Article  Google Scholar 

  • Vickers T (1985) Embryolethality in rats caused by retinoic acid. Teratology 31(1):19–33

    Article  CAS  PubMed  Google Scholar 

  • Villalobos SA, Hamm JT, Teh SJ, Hinton DE (2000) Thiobencarb-induced embryotoxicity in medaka (Oryzias latipes): stage-specific toxicity and the protective role of chorion. Aquat Toxicol 48(2):309–326

    Article  CAS  PubMed  Google Scholar 

  • Vito CC, Wieland SJ, Fox TO (1979) Androgen receptors exist throughout the ‘critical period’of brain sexual differentiation. Nature 282:308–310

    Article  CAS  PubMed  Google Scholar 

  • Wangensteen OD, Rahn H, Burton RR, Smith AH (1974) Respiratory gas exchange of high altitude adapted chick embryos. Respir Physiol 21(1):61–70

    Article  CAS  PubMed  Google Scholar 

  • Weber LP, Hill RL Jr, Janz DM (2003) Developmental estrogenic exposure in zebrafish (Danio rerio): II. Histological evaluation of gametogenesis and organ toxicity. Aquat Toxicol 63(4):431–446

    Article  CAS  PubMed  Google Scholar 

  • Wedemeyer G (1968) Uptake and distribution of Zn65 in the coho salmon egg (Oncorhynchus kisutch). Comp Biochem Physiol 26(1):271–279

    Article  CAS  Google Scholar 

  • Wibbels T, Bull JJ, Crews D (1991) Chronology and morphology of temperature-dependent sex determination. J Exp Zool 260(3):371–381

    Article  CAS  PubMed  Google Scholar 

  • Williams W (2001) Anthropogenic salinisation of inland waters. Hydrobiologia 466:329–337

    Article  Google Scholar 

  • Wong C, Chu K, Tang K, Tam T, Wong L (1993) Effects of chromium, copper and nickel on survival and feeding behaviour of Metapenaeus ensis larvae and postlarvae (Decapoda: Penaeidae). Mar Environ Res 36(2):63–78

    Article  CAS  Google Scholar 

  • Wong-Riley MT, Liu Q (2005) Neurochemical development of brain stem nuclei involved in the control of respiration. Respir Physiol Neurobiol 149(1):83–98

    Article  CAS  PubMed  Google Scholar 

  • Wu Y, Zhou Q (2012) Dose- and time-related changes in aerobic metabolism, chorionic disruption, and oxidative stress in embryonic medaka (Oryzias latipes): underlying mechanisms for silver nanoparticle developmental toxicity. Aquat Toxicol 124–125(0):238–246

    Article  PubMed  CAS  Google Scholar 

  • Xu L, Mortola JP (1989) Effects of hypoxia or hyperoxia on the lung of the chick embryo. Can J Physiol Pharmacol 67(5):515–519

    Article  CAS  PubMed  Google Scholar 

  • Yntema C (1968) A series of stages in the embryonic development of Chelydra serpentina. J Morphol 125(2):219–251

    Article  CAS  PubMed  Google Scholar 

  • Yntema C (1976) Effects of incubation temperatures on sexual differentiation in the turtle, Chelydra serpentina. J Morphol 150(2):453–461

    Article  CAS  PubMed  Google Scholar 

  • Yntema C (1979) Temperature levels and periods of sex determination during incubation of eggs of Chelydra serpentina. J Morphol 159(1):17–27

    Article  CAS  PubMed  Google Scholar 

  • Yntema C, Mrosovsky N (1982) Critical periods and pivotal temperatures for sexual differentiation in loggerhead sea turtles. Can J Zool 60(5):1012–1016

    Article  Google Scholar 

  • Yuan J, Zhang X, Yu L, Sun Z, Zhu P, Wang X, Shi H (2011) Stage-specific malformations and phenotypic changes induced in embryos of amphibian (Xenopus tropicalis) by triphenyltin. Ecotoxcol Environ Safe 74(7):1960–1966

    Article  CAS  Google Scholar 

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Mueller, C.A. (2018). Critical Windows in Animal Development: Interactions Between Environment, Phenotype, and Time. In: Burggren, W., Dubansky, B. (eds) Development and Environment. Springer, Cham. https://doi.org/10.1007/978-3-319-75935-7_3

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