Incubation temperature affects the expression of young precocial birds’ fear-related behaviours and neuroendocrine correlates

The influence of embryonic microclimate on the behavioural development of birds remains unexplored. In this study, we experimentally tested whether chronic exposure to suboptimal temperatures engendered plasticity in the expression of fear-related behaviours and in the expression of the corticotropin-releasing factor in the brains of domestic chicks (Gallus g. domesticus). We compared the neurobehavioural phenotypes of a control group of chicks incubated in an optimal thermal environment (37.8 °C) with those of a group of experimental chicks exposed chronically in ovo to suboptimal temperatures (27.2 °C for 1 hour twice a day). Chronic exposure to a suboptimal temperature delayed hatching and decreased growth rate and experimental chicks had higher neophobic responses than controls in novel food and novel environment tests. In addition, experimental chicks showed higher expression of corticotropin-releasing factor than did controls in nuclei of the amygdala, a structure involved in the regulation of fear-related behaviours. In this study, we report the first evidence of the strong but underappreciated role of incubation microclimate on the development of birds’ behaviour and its neurobiological correlates.

• Publication year

  2018

• Venue

  Scientific Reports

• Publication date

  2018-01-30

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1038/s41598-018-20319-yPMID 29382895PMCID 5789981
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Nest-box temperature affects clutch size, incubation initiation, and nestling health in great tits

  2017cited by this paper
• Climate change and nesting behaviour in vertebrates: a review of the ecological threats and potential for adaptive responses

  2017cited by this paper
• The impact of egg incubation temperature on the personality of oviparous reptiles

  2016cited by this paper
• Effects of Cool Nest Microclimates on Nestling Development: An Experimental Study with Mediterranean Great Tits Parus major

  2016cited by this paper
• Multiple amygdaloid divisions of arcopallium send convergent projections to the nucleus accumbens and neighboring subpallial amygdala regions in the domestic chicken: a selective pathway tracing and reconstruction study

  2016cited by this paper
• The behavioural and physiological strategies of bird and reptile embryos in response to unpredictable variation in nest temperature

  2015cited by this paper
• Egg Cortisol Exposure Enhances Fearfulness in Larvae and Juvenile Rainbow Trout

  2015cited by this paper
• Individual variation in the oxidative costs of personality traits

  2015cited by this paper
• Artificially Increased Yolk Hormone Levels and Neophobia in Domestic Chicks

  2015cited by this paper
• Predator-Specific Effects on Incubation Behaviour and Offspring Growth in Great Tits

  2015cited by this paper
• Influence of incubation temperature on offspring phenotype and fitness in birds

  2015cited by this paper
• Egg quality, embryonic development, and post-hatching phenotype: an integrated perspective

  2015cited by this paper
• Oxidative Stress and Hormesis in Evolutionary Ecology and Physiology

  2014cited by this paper
• Can environmental conditions experienced in early life influence future generations?

  2014cited by this paper
• Exposure of embryos to cyclically cold incubation temperatures durably affects energy metabolism and antioxidant pathways in broiler chickens.

  2014cited by this paper
• Steroid extraction: Get the best out of faecal samples

  2013cited by this paper
• The CRF system and social behavior: a review

  2013cited by this paper
• Trans-generational effects of prenatal stress in quail

  2013cited by this paper
• Ecological, evolutionary, and conservation implications of incubation temperature‐dependent phenotypes in birds

  2013cited by this paper
• Personality Traits and Behavioral Syndromes in Differently Urbanized Populations of House Sparrows (Passer domesticus)

  2012cited by this paper
• Hotter nests produce smarter young lizards

  2012cited by this paper
• Monitoring stress hormone metabolites as a useful, non-invasive tool for welfare assessment in farm animals

  2012cited by this paper
• Incubation Temperature Affects Growth and Energy Metabolism in Blue Tit Nestlings

  2011cited by this paper
• Embryonic Developmental Patterns and Energy Expenditure Are Affected by Incubation Temperature in Wood Ducks (Aix sponsa)

  2011cited by this paper
• Slight differences in incubation temperature affect early growth and stress endocrinology of wood duck (Aix sponsa) ducklings

  2010cited by this paper
• Thermal Acclimation of Heart Rates in Reptilian Embryos

  2010cited by this paper
• Experimental cooling during incubation leads to reduced innate immunity and body condition in nestling tree swallows

  2010cited by this paper
• Unusual Incubation Behavior and Embryonic Tolerance of Hypothermia by the Blood Pheasant (Ithaginis cruentus)

  2010cited by this paper
• Social motivation affects the display of individual discrimination in young and adult Japanese quail (Coturnix japonica).

  2009cited by this paper
• Oxidative damage in different tissues of neonatal chicks exposed to low environmental temperature.

  2009cited by this paper
• Experimental reduction of incubation temperature affects both nestling and adult blue tits Cyanistes caeruleus

  2008cited by this paper
• Variation in maternal effects and embryonic development rates among passerine species

  2008cited by this paper
• Ontogeny of vocalizations and movements in response to cooling in chickens fetuses.

  2007cited by this paper
• GEOGRAPHIC VARIATION IN AVIAN INCUBATION PERIODS AND PARENTAL INFLUENCES ON EMBRYONIC TEMPERATURE

  2007cited by this paper
• Maternal effects in Wood Ducks: incubation temperature influences incubation period and neonate phenotype

  2006cited by this paper
• The effects of suboptimal eggshell temperature during incubation on broiler chick quality, live performance, and further processing yield.

  2006cited by this paper
• Noninvasive Heart Rate Measurement Using a Digital Egg Monitor in Chicken and Turkey Embryos

  2006cited by this paper
• Periodic Cooling of Bird Eggs Reduces Embryonic Growth Efficiency

  2006cited by this paper
• Physiological and Behavioral Differences in Magellanic Penguin Chicks in Undisturbed and Tourist‐Visited Locations of a Colony

  2005cited by this paper
• The effects of rearing temperature on developmental stability and learning and memory in the honey bee, Apis mellifera

  2005cited by this paper
• Maternal hormones as a tool to adjust offspring phenotype in avian species.

  2005cited by this paper
• The developmental origins of the metabolic syndrome.

  2004cited by this paper
• Revised nomenclature for avian telencephalon and some related brainstem nuclei

  2004cited by this paper
• Measurement of corticosterone metabolites in chicken droppings

  2004cited by this paper
• Distribution of corticotropin‐releasing factor‐immunoreactive neurons in the central nervous system of the domestic chicken and Japanese quail

  2004cited by this paper
• Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype.

  2004cited by this paper
• Avian Incubation: Behaviour, Environment, and Evolution

  2003cited by this paper
• Ecological Aspects of Neophobia and Neophilia in Birds

  2001cited by this paper
• The costs of egg production and incubation in great tits (Parus major)

  2001cited by this paper
• Resource allocation between reproductive phases: the importance of thermal conditions in determining the cost of incubation

  2000cited by this paper
• Early development and fitness in birds and mammals.

  1999cited by this paper
• Maternal effects as adaptations

  1998cited by this paper
• Hypothermic tolerance in an embryonic American kestrel (Falco sparverius)

  1998cited by this paper
• Fear and adaptability in poultry: insights, implications and imperatives

  1996cited by this paper
• The effect of archistriatal lesions on 'open field' and fear/avoidance behaviour in the domestic chick.

  1995cited by this paper
• Effects of CRF on isolated Japanese quails selected for fearfulness and for sociality.

  1993cited by this paper
• Poultry production systems. Behaviour, management and welfare

  1993cited by this paper
• Research note: open-field behavior of Japanese quail chicks genetically selected for low or high plasma corticosterone response to immobilization stress.

  1992cited by this paper
• Lesions of the central nucleus of the amygdala, but not the paraventricular nucleus of the hypothalamus, block the excitatory effects of corticotropin-releasing factor on the acoustic startle reflex

  1992cited by this paper
• A stereotaxic atlas of the brain of the chick (Gallus domesticus)

  1988cited by this paper
• Thermal Tolerance of Avian Embryos: A Review

  1987cited by this paper
• Response of egg temperature, heart rate and blood pressure in the chick embryo to hypothermal stress

  1985cited by this paper
• Localization of corticotropin-releasing factor-containing neurons in the brain of the domestic fowl

  1984cited by this paper
• The Role of Neophobia in Determining the Degree of Foraging Specialization in Some Migrant Warblers

  1983cited by this paper
• Nest Inattentiveness and Its Influence on Development of the Young in the Superb Lyrebird

  1979cited by this paper
• Egg Neglect in the Procellariiformes: Reproductive Adaptations in the Fork-Tailed Storm-Petrel

  1979cited by this paper
• Responses of domestic fowl to novel food and objects

  1977cited by this paper
• Egg temperature and incubation rhythm of a Capercaillie (Tetrao urogallus L.) in Swedish Lapland

  1966cited by this paper
• Effect of Temperature, Humidity, and Other Factors on Hatch of Hens' Eggs and on Energy Metabolism of Chick Embryos

  1937cited by this paper

• Reproductive characteristics of Japanese quail hatched from eggs incubated at different temperatures.

  2025cites this paper
• Effects of the temperature during embryonic development on adult reproduction and the phenotype of the second generation in zebra finches.

  2024cites this paper
• Embryonic thermal manipulation: a potential strategy to mitigate heat stress in broiler chickens for sustainable poultry production

  2024influential citation
• Animal welfare of embryos and newly hatched chicks: A review

  2023cites this paper
• Parental behavior and newborn attachment in birds: life history traits and endocrine responses

  2023cites this paper
• Temperature during embryonic development in brown trout influences juvenile behaviour in encounters with predators

  2023cites this paper
• Incubation as a driver of maternal effects: Temperature influences levels of yolk maternally derived 5α-dihydrotestosterone.

  2023cites this paper
• Suboptimal Embryonic Incubation Temperature Has Long-Term, Sex-Specific Consequences on Beak Coloration and the Behavioral Stress Response in Zebra Finches

  2022cites this paper
• A novel male Japanese quail structural connectivity atlas using ultra-high field diffusion MRI at 11.7 T

  2022cites this paper
• Increased temperature during incubation increases the sociality of male broilers in later life

  2022cites this paper
• Early Phenotype Programming in Birds by Temperature and Nutrition: A Mini-Review

  2022cites this paper
• Effect of lower temperature stimuli during incubation on fear and social-related behaviours in broilers

  2022cites this paper
• Dabbling Duck Eggs Hatch after Nest Abandonment in the Wild

  2022cites this paper
• Ecological footprint of poultry production and effect of environment on poultry genes

  2022cites this paper
• Comparison of Some Behavioural Responses in Budgerigars (Melopsittacus undulatus) Raised in Cages Enriched with Coloured LED Lights

  2022cites this paper
• Design and economic analysis of a solar poultry incubator for rural sectors located in Pucallpa-Peru

  2022cites this paper
• No trans-generational maternal effects of early-life corticosterone exposure on neophobia and antipredator behaviour in the house sparrow

  2021cites this paper
• Prenatal and Early Postnatal Behavioural Programming in Laying Hens, With Possible Implications for the Development of Injurious Pecking

  2021cites this paper
• Incubation Temperature Affects Duckling Body Size and Food Consumption Despite No Effect on Associated Feeding Behaviors

  2020cites this paper
• Short cold exposures during incubation and postnatal cold temperature affect performance, breast meat quality, and welfare parameters in broiler chickens

  2020cites this paper
• Comparative assessment of general behaviour and fear-related responses in hatchery-hatched and on-farm hatched broiler chickens

  2020cites this paper
• Early chronic hypoxia does not impact rainbow trout behaviour later in life

  2020cites this paper
• Incubation temperature and PCB-126 exposure interactively impair shorebird embryo and post-hatch development.

  2020cites this paper
• Parental effects and climate change: Will avian incubation behavior shield embryos from increasing environmental temperatures?

  2019cites this paper
• Exposure of Avian Embryos to Cycling Incubation Temperatures Reduces Adult Bactericidal Ability

  2019cites this paper
• Mercury Exposure and Altered Parental Nesting Behavior in a Wild Songbird.

  2019cites this paper
• Nest microclimate during incubation affects posthatching development and parental care in wild birds

  2019cites this paper
• Human behaviour at the origin of maternal effects on offspring behaviour in laying hens (Gallus gallus domesticus).

  2019cites this paper
• Object and food novelty induce distinct patterns of c-fos immunoreactivity in amygdala and striatum in domestic male chicks (Gallus gallus domesticus).

  2019cites this paper
• Behaviour, physiology and body mass of Nigerian indigenous hens during brooding

  2019influential citation
• Behavioural repeatability is affected by early developmental conditions in a butterfly

  2019cites this paper
• The Interactive Effects of Incubation Temperature and Organic Contaminants on Shorebird Embryo Development

  2019influential citation
• Egg incubation temperature affects the timing of the Atlantic salmon Salmo salar homing migration.

  2018cites this paper