Developmental stress reduces body condition across avian life-history stages: A comparison of quantitative magnetic resonance data and condition indices

https://doi.org/10.1016/j.ygcen.2018.11.008Get rights and content

Highlights

  • Developmental CORT reduces nestling body mass and body size.

  • Effects of developmental CORT treatment on body size last into adulthood.

  • Popular condition indices are not good predictors of nestling relative body fat.

Abstract

Animals exposed to stressful developmental conditions can experience sustained physiological, behavioral, and fitness effects. While extensive research shows how developmental stress affects development, few studies have examined the effects on body composition. To test the effects of developmental stress on nestling and adult body composition, we dosed nestling zebra finches (Taeniopygia guttata) with either a corticosterone (CORT) or control treatment. We calculated condition indices (scaled mass, residual mass, and ratio indices) from morphometric measurements and used quantitative magnetic resonance (QMR) to assess body composition during early development and adulthood. We compared these three traditionally-used condition indices to QMR-derived body composition measurements, to test how well they predict relative fat mass. Our results show that developmental stress decreases body mass, and has a dose-dependent effect on tarsus length in nestling birds. Furthermore, stress treatment during the nestling period had long-lasting effects on adult body mass, lean mass and tarsus length. None of the three condition indices were good indicators of relative fat mass in nestlings, but all indices were closely associated with relative fat mass in adults. The scaled mass index was more closely associated with relative fat mass than the other condition indices, when calculated from wing chord length in nestlings. In adults however, the residual mass index and the ratio index were better indicators of relative body fat than the scaled mass index, when calculated from tarsus length. Our data demonstrate the short and long-term impact of developmental stress on birds, and highlight important age-related factors to consider when using condition indices.

Introduction

The environment animals experience during development can have sustained effects on their morphology, physiology, behavior, and fitness (Chaby, 2016, Lindstrom, 1999, Lupien et al., 2009, Schoech et al., 2011). For example, in birds, developmental stress decreases nestling growth and body size (Coslovsky and Richner, 2011, Crino et al., 2014, Merino and Potti, 1995, Schmidt et al., 2012). In birds, these effects can have consequences for behavior, longevity, and fitness later in life (Krause and Naguib, 2011, Metcalfe and Monaghan, 2001), which may be mediated in part by compensatory growth (Metcalfe and Monaghan, 2001).

Many studies have examined the impact of stress on nestling development, with mixed results as to the long- and short-term effects of stress on body mass (e.g. Crino et al., 2014, Naguib and Gil, 2005, Schmidt et al., 2012), but only a few have examined effects on nestling body composition (Farrell et al., 2015, Kriengwatana et al., 2013, Schmidt et al., 2012). Clutch size and food restriction have long-lasting effects (present in adults that were treated as nestlings) on body mass and body composition, which suggests that long-term changes in morphology can occur due to early life conditions (Kriengwatana et al., 2013, Naguib and Gil, 2005). However, the manipulations used in these studies directly or indirectly (through sibling competition) alter food access to the nestlings. While food restriction can elevate stress hormone levels (Lynn et al., 2003), food restriction may confound the effects of stress on morphology by directly limiting nestling growth. Stress treatment without food restriction has been shown to reduce nestling mass and affect body composition beyond the end of the treatment, but not into adulthood (Crino et al., 2014, Schmidt et al., 2012). Hence, there is no consensus as to whether developmental stress can have long-lasting effects on nestling body mass, body composition, and body condition.

Body condition is an ecologically important concept that is widely used in physiology, behavior, and ecology studies to evaluate the health and well-being of animals (e.g. Booth and Hixon, 1999, Jakob et al., 1996, Rowe and Houle, 1996, Wauters et al., 1995). Condition is a measure of the energetic or nutritional state of an animal, and is commonly defined as the relative size of energy reserves (i.e. relative fat mass) that an animal has available to allocate to life processes (e.g. daily maintenance, reproduction, immunocompetence; Hill, 2011, Jacobs et al., 2012, Schulte-Hostedde et al., 2001). This definition has received criticism for a number of reasons. Both fat and lean tissue (i.e. muscle) may be important for animal performance and fitness (Gerson and Guglielmo, 2011, Hedenström et al., 2009). Additionally, an animal’s optimal body composition may vary across life-history stages. For example, in small passerines, larger fat stores may be beneficial for thermoregulation (Bednekoff et al., 1994), and are linked to nestling survival (Tinbergen and Boerlijst, 1990), but could be a hindrance during fledging when body mass can be a detriment to take-off flight (Kullberg et al., 1996, Sprague and Breuner, 2010).

Condition indices such as the scaled mass index, residual mass index, and ratio index are calculated from body measurements (i.e. mass, length etc; Maute et al., 2015, McWilliams and Whitman, 2013, Peig and Green, 2010) and are commonly used to estimate body condition in both adults and developing animals (Golet and Irons, 1999, Jakob et al., 1996, Schulte-Hostedde et al., 2001, Sockman and Schwabl, 2001). The scaled mass index accounts for errors associated with the dependency between length and body mass measurements and is considered by some to be a more accurate measure of condition than the residual body mass index and the ratio index (Bókony et al., 2012; but see Jacobs et al., 2012, Labocha et al., 2014). However, all three indices are widely used across taxonomic groups to quantify condition (Falk et al., 2017, Labocha et al., 2014, MacCracken and Stebbings, 2012). Condition indices rely on the assumption that increased relative body mass is equivalent to increased relative body fat (Hill, 2011, McWilliams and Whitman, 2013), but changes in body mass can occur due to changes in lean mass (Gerson and Guglielmo, 2011, Hedenström et al., 2009, McWilliams and Whitman, 2013). Here, we use quantitative magnetic resonance (QMR) to directly evaluate changes in body composition over life-history stages in zebra finches (Taeniopygia guttata) exposed to either a stress hormone, corticosterone (CORT), or control treatment (peanut oil) during development. We then compared QMR body composition data to three commonly used condition indices, to test whether these indices accurately represent relative fat mass in nestlings.

QMR is a relatively new technique for measuring body composition (EchoMRI™, 2016). It uses a magnetic field to align the spins of hydrogen nuclei, and estimates the amount of different tissue types (e.g. lean muscle, fatty tissue, etc.) based on the frequencies at which these hydrogen nuclei resonate in the sample (EchoMRI™, 2016, Guglielmo et al., 2011). Unlike some other magnetic resonance methods (such as MRI), QMR gives a value of the total mass of different tissues, but does not give a visual estimation of the distribution of tissues in the body (Guglielmo et al., 2011, Hedenström et al., 2009). QMR has been validated as a method of measuring body composition in birds by comparing QMR measurements to gravimetric analyses of carcasses (Guglielmo et al., 2011), and has been used in studies of both wild (Kennedy et al., 2016, Seewagen and Guglielmo, 2011) and captive birds (Farrell et al., 2015, Schmidt et al., 2012). Whereas traditional methods of evaluating whole animal body composition, such as bomb calorimetry, require destruction of the study animal, QMR provides an accurate assessment of soft tissue composition without harming the animal, allowing for longitudinal studies (Johnson et al., 2009, McWilliams and Whitman, 2013, Riley et al., 2016, Warner et al., 2016).

The goals of this study were threefold: 1) To quantify the effects of developmental stress on nestling body composition using QMR, 2) To determine if the effects of developmental stress on body composition persist to adulthood, and 3) To compare QMR measures of body composition to traditional condition indices (the scaled mass, residual body mass, and ratio indices). To accomplish this, we exposed nestling zebra finches to a physiologically relevant high or low dose of CORT or control treatment, and compared changes in body composition between experimental and control nestlings. We made the same comparison with a subset of adult birds that had received either a high-dose CORT treatment or control treatment. We predicted that CORT treatment would decrease nestling body mass and body fat, with more pronounced effects in the high-dose CORT treatment, but that there would be no/less effect on lean mass (in accordance with Farrell et al., 2015). We also predicted that there would be no differences in body mass or composition between the treatments by adulthood (Farrell et al., 2015, Schmidt et al., 2012). Finally, we predicted that condition indices would reflect the body fat of the nestlings more closely than lean mass, and that the scaled mass index (considered to be a more accurate estimate of condition, Peig and Green, 2009, Peig and Green, 2010) would reflect fat mass more closely than the other two indices (but see Jacobs et al., 2012, Labocha et al., 2014).

Section snippets

Parental birds - housing and breeding

From December 2015 to November 2016, adult zebra finches were sourced from an existing breeding colony of wild-derived (12–14 generations from wild) zebra finches at Deakin University, Waurn Ponds, Australia. Eight pairs of zebra finches were each housed in four indoor flight cages measuring 3 × 1 × 2 meters, for a total of 32 breeding pairs used in the experiment. We housed birds on a 14:10 light/dark cycle at 20 °C (±1 °C) with 50% humidity. We provided breeding birds with ad libitum

Nestling condition and developmental CORT

CORT treatment during development decreased nestling mass, tarsus length and ratio index value (Table 1, Supplementary material Table s2). CORT treatment did not affect any other body condition variable in nestlings. Post-hoc tests showed that there was a dose-dependent effect on tarsus length, such that birds from the high dose treatment had smaller tarsi compared to the low dose treatment group (Table 2).

Nestlings gained body mass, lean mass, relative lean mass, tarsus length, and increased

Condition and CORT treatment

The effects of stress during early development on nestling body mass are well documented and robust (Naguib et al., 2004, Spencer et al., 2003). Here, we confirm that CORT treatment during development decreases nestling body size (mass and tarsus length), with a dose-dependent effect on nestling tarsus length. Interestingly, some of these effects persisted into adulthood, with high-dose CORT-treated nestlings having lower body mass, lower lean mass and shorter tarsus length as adults. Finally,

Summary and conclusions

In our experiment, developmental stress decreased body mass and body size in nestlings, and had lasting effects on body mass, lean mass and tarsus length across life history stages. More studies are needed to determine whether the effects seen in nestlings and adults have long-term consequences for reproductive success and survival, and whether the effects of stress are ultimately detrimental or adaptive. We found the scaled mass index was the best performing condition index for nestlings.

Acknowledgements

This work was supported by the Australian Research Council Future Fellowship [FT140100131 to K.L.B.]. These experiments were conducted under the ethics permit G15-2015 and was approved by Animal Ethics Committee Laboratory-Geelong (AECL-G). We thank the Deakin Waurn Ponds Campus animal care staff, especially Dr. Rod Collins. We also thank two anonymous reviewers for their comments which helped to improve the quality of this manuscript.

References (66)

  • S.E. Lynn et al.

    Short-term fasting affects locomotor activity, corticosterone, and corticosterone binding globulin in a migratory songbird

    Horm. Behav.

    (2003)
  • N.B. Metcalfe et al.

    Compensation for a bad start: grow now, pay later?

    TREE

    (2001)
  • D. Rubolini et al.

    Effects of elevated egg corticosterone levels on behavior, growth, and immunity of yellow-legged gull (Larus michahellis) chicks

    Horm. Behav.

    (2005)
  • K.W. Sockman et al.

    Plasma corticosterone in nestling american kestrels: effects of age, handling stress, yolk androgens, and body condition

    Gen. Comp. Endocrinol.

    (2001)
  • K.A. Spencer et al.

    Song as an honest signal of developmental stress in the zebra finch (Taeniopygia guttata)

    Horm. Behav.

    (2003)
  • K.A. Spencer et al.

    Delayed behavioral effects of postnatal exposure to corticosterone in the zebra finch (Taeniopygia guttata)

    Horm. Behav.

    (2007)
  • R.S. Sprague et al.

    Timing of fledging is influenced by glucocorticoid physiology in Laysan Albatross chicks

    Horm. Behav.

    (2010)
  • L.B. Astheimer et al.

    Interactions of corticosterone with feeding, activity and metabolism in passerine birds

    Ornis Scandinavica (Scandinavian J. Ornithol.)

    (1992)
  • P.A. Bednekoff et al.

    Great tit fat reserves under unpredictable temperatures

    J. Avian Biol.

    (1994)
  • D.J. Booth et al.

    Food ration and condition affect early survival of the coral reef damselfish

    Stegastes partitus Oecologia

    (1999)
  • K.L. Buchanan et al.

    Song as an honest signal of past developmental stress in the European starling (Sturnus vulgaris)

    Proc. Biol. Sci.

    (2003)
  • E.H. Chin et al.

    Juveniles exposed to embryonic corticosterone have enhanced flight performance

    Proc. R Soc. B: Biol. Sci.

    (2009)
  • M. Coslovsky et al.

    Predation risk affects offspring growth via maternal effects

    Funct. Ecol.

    (2011)
  • B. Diedenhofen et al.

    cocor: a comprehensive solution for the statistical comparison of correlations

    PLoS One

    (2015)
  • EchoMRI™, 2016. About...
  • B.G. Falk et al.

    A validation of 11 body-condition indices in a giant snake species that exhibits positive allometry

    PLoS One

    (2017)
  • A.R. Gerson et al.

    Flight at low ambient humidity increases protein catabolism in migratory birds

    Science

    (2011)
  • H.G. Golet et al.

    Raising young reduces body condition and fat stores in black-legged kittiwakes

    Oecologia

    (1999)
  • C.G. Guglielmo et al.

    Simple, rapid, and non-invasive measurement of fat, lean, and total water masses of live birds using quantitative magnetic resonance

    J. Ornithol.

    (2011)
  • A. Hedenström et al.

    Magnetic resonance Imaging versus chemical fat extraction in a small passerine, the willow warblerPhylloscopus trochilus: a fat-score based statistical comparison

    J. Avian Biol.

    (2009)
  • G.E. Hill

    Condition-dependent traits as signals of the functionality of vital cellular processes

    Ecol. Lett.

    (2011)
  • S.R. Jacobs et al.

    Determining seabird body condition using nonlethal measures

    Physiol. Biochem. Zool.

    (2012)
  • E.M. Jakob et al.

    Estimating fitness: a comparison of body condition indices

    Oikos

    (1996)
  • Cited by (24)

    • Mitochondria as the powerhouses of sexual selection: Testing mechanistic links between development, cellular respiration, and bird song

      2022, Hormones and Behavior
      Citation Excerpt :

      Additionally, developmentally induced changes in mitochondrial function that affect body size and condition could affect song in adult birds by changing the ability to produce energy needed to perform song displays and/or by changing motor performance (Koch and Hill, 2018). For example, exposure to elevated CORT during development decreases growth and can have lasting effects on adult body size (Crino et al., 2014a; Kraft et al., 2019). Song frequency can be affected by muscle performance, body size, and morphology, and is likely under sexual selection, given its robust relationship with sexual size dimorphism (Francis and Wilkins, 2021; Friis et al., 2021; Mikula et al., 2021; Podos, 2001).

    • Developmental conditions have intergenerational effects on corticosterone levels in a passerine

      2021, Hormones and Behavior
      Citation Excerpt :

      In addition, there are cases where prenatal exposure to elevated CORT (Coturnix japonica, Zimmer et al., 2013) and maltreatment during early development (Sula granti, Grace and Anderson, 2018) have resulted in depressed glucocorticoid levels later in life. Exposure to glucocorticoids during development can affect many other traits that influence fledgling survival (e.g. growth, Hayward and Wingfield, 2004, and begging rate, Loiseau et al., 2008), and it has been shown to decrease growth and final adult size and body condition in zebra finches (Taeniopygia guttata, Kraft et al., 2019). Although the relationships between glucocorticoids and fitness are highly variable and dependent on the life history of the species (Schoenle et al., 2021), baseline and peak glucocorticoids can affect both survival and reproductive success in wild animals (Blas et al., 2007, Ethan Pride, 2005, reviewed in Bonier et al., 2009, Schoech et al., 2011).

    • Selective logging reduces body size in omnivorous and frugivorous tropical forest birds

      2021, Biological Conservation
      Citation Excerpt :

      Nutritional restrictions and other stressful events experienced during early-life development can reduce growth rate, so that individuals are of smaller body size in adulthood. For example, artificially induced developmental stress through corticosterone administration constrained tarsus growth in nestling common kestrels (Falco tinnunculus) and in zebra finches (Taeniopygia guttata) (Kraft et al., 2019; Muller et al., 2009). Such phenotypic effects are not necessarily negative.

    • Frog somatic indices: Importance of considering allometric scaling, relation with body condition and seasonal variation in the frog Leptodactylus latrans

      2020, Ecological Indicators
      Citation Excerpt :

      However, in a recent study on the frog Leptodactylus latrans, our group demonstrated that a truly size-independent SMI value is better obtained by defining the scaling exponent through a non-linear regression of mass on length rather than by performing a standardized major axis regression of lnweight on lnlength (Brodeur et al., 2020). The SMI gradually gained popularity in various disciplines as a body condition index, and has now been successfully employed in studies with fish (Maceda-Veiga et al., 2014; Brodeur et al., 2017; Dalzochio et al., 2018; Wuenschel et al., 2019), birds (Hudin et al., 2016; Nip et al., 2018; Fanny-Linn et al., 2019; English et al., 2018), mammals (Tête et al., 2013; Rodríguez-Estival and Smits, 2016; Abolins et al., 2018; Risco et al., 2018), and amphibians (MacCracken and Stebbings, 2012; Sánchez et al., 2013; Alvarado-Rybak et al., 2018; Romano et al., 2018; Brodeur et al., 2020). However, although the necessity to consider the allometric scaling of growth is widely recognized when calculating the whole body condition index, many researchers still disregard the fact that allometric growth also occurs at the organ level.

    View all citing articles on Scopus
    View full text