J Comp Physiol B (2013) 183:821–831 DOI 10.1007/s00360-013-0751-6
ORIGINAL PAPER
Catch-up growth in Japanese quail (Coturnix Japonica): relationships with food intake, metabolic rate and sex Eunice H. Chin • Andrea L. Storm-Suke Ryan J. Kelly • Gary Burness
•
Received: 26 September 2012 / Revised: 1 March 2013 / Accepted: 4 March 2013 / Published online: 28 March 2013 Ó Springer-Verlag Berlin Heidelberg 2013
Abstract The effects of early environmental conditions can profoundly affect individual development and adult phenotype. In birds, limiting resources can affect growth as nestlings, but also fitness and survival as adults. Following periods of food restriction, individuals may accelerate development, undergoing a period of rapid ‘‘catch-up’’ growth, in an attempt to reach the appropriate size at adulthood. Previous studies of altricial birds have shown that catch-up growth can have negative consequences in adulthood, although this has not been explored in species with different developmental strategies. Here, we investigated the effects of resource limitation and the subsequent period of catch-up growth, on the morphological and metabolic phenotype of adult Japanese quail (Coturnix japonica), a species with a precocial developmental strategy. Because males and females differ in adult body size, we also test whether food restriction had sex-specific effects. Birds that underwent food restriction early in development had muscles of similar size and functional maturity, but lower adult body mass than controls. There was no evidence of sex-specific sensitivity of food restriction on adult body mass; however, there was evidence for body size. Females fed ad lib were larger than males fed ad lib, while females subjected to food restriction
Communicated by G. Heldmaier. E. H. Chin (&) A. L. Storm-Suke Environmental and Life Sciences Graduate Program, Trent University, 1600 West Bank Drive, Peterborough, ON K9J 7B8, Canada e-mail:
[email protected] R. J. Kelly G. Burness Department of Biology, Trent University, 1600 West Bank Drive, Peterborough, ON K9J 7B8, Canada
were of similar size to males. Adults that had previously experienced food restriction did not have an elevated metabolic rate, suggesting that in contrast to altricial nestlings, there was no metabolic carry-over effect of catch-up growth into adulthood. While Japanese quail can undergo accelerated growth after re-feeding, timing of food restriction may be important to adult size, particularly in females. However, greater developmental flexibility compared to altricial birds may contribute to the lack of metabolic carryover effects at adulthood. Keywords Catch-up growth Metabolic rate Early environment
Introduction Poor nutrition early in life may affect the ability of an individual to cope with different environments at adulthood (Monaghan 2008). It is increasingly recognized that, across taxa, individuals may be capable of adjusting phenotypic development to alleviate some of the potentially negative effects of poor nutrition during early development (Bateson et al. 2004). For example, following a period of resource restriction whereby growth is depressed, individuals may accelerate their growth upon re-feeding, in an attempt to reach the appropriate size at adulthood (Hector and Nakagawa 2012). Such a strategy of ‘‘catch-up’’ growth has been observed across numerous taxa (e.g. ladybugs: Dmitriew and Rowe 2011; fish: Auer et al. 2010; Oh et al. 2008; reptiles: Radder et al. 2007; Roark et al. 2009; birds: Blount et al. 2006; Criscuolo et al. 2008). However, catchup growth may have metabolic consequences, and possibly negative effects on fitness (Auer et al. 2010; JimenezChillaron and Patti 2007; Mangel and Munch 2005;
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Metcalfe and Monaghan 2001, 2003; Yearsley et al. 2004). For example in birds, zebra finch (Taeniopygia guttata) juveniles fed a low quality diet (i.e. low protein) during the first month of life, and that underwent catch-up growth, had elevated resting metabolic rates (RMR) as adults (Criscuolo et al. 2008); a greater decline of flight performance post-breeding (Criscuolo et al. 2011); delayed onset and slower rate of egg laying (Blount et al. 2006); and increased susceptibility to oxidative damage (AlonsoAlvarez et al. 2007) compared with control individuals. Similarly, individuals raised with increased sibling competition (a resource-poor environment) (Verhulst et al. 2006) or restricted resources (Schmidt et al. 2012) demonstrated higher RMR at adulthood. Together, the study of Criscuolo et al. (2008), that of Verhulst et al. (2006) and Schmidt et al. (2012), suggests that early rearing environment can impact adult energy expenditure. However, a subsequent study of zebra finches did not detect an increased RMR in adults that had experienced catch-up growth during development, although individuals raised on a low protein diet had increased exploratory and foraging behaviours (Krause and Naguib 2011). Males and females may differ in their responses to poor environmental conditions during development, especially in species that display sexual size dimorphism as adults (Jones et al. 2009; Ra˚berg et al. 2005). Studies reporting sex-specific sensitivity have traditionally reported the larger sex to be more negatively affected by poor environmental conditions (Chin et al. 2005; Fargallo et al. 2002; Hipkiss et al. 2002; Laaksonen et al. 2005; Torres and Drummond 1997; Velando 2002), possibly due to an inability of parents to provide sufficient resources for the larger sex when resources are limited (Anderson et al. 1993; Torres and Drummond 1999; Velando 2002). In other species, the smaller sex may have increased sensitivity (e.g. Dubiec et al. 2006; Verhulst et al. 2006), suggesting that multiple variables may contribute to sex-specific sensitivity to early environmental conditions (e.g., Ra˚berg et al. 2005; Jones et al. 2009). Studies considering catch-up growth in birds within an evolutionary context have primarily focused on altricial species (Birkhead et al. 1999; Criscuolo et al. 2008; Honarmand et al. 2010) (but see Schew 1995; Zhan et al. 2007). Altricial birds hatch naked and blind, are nestbound and completely dependent on their parents for food (Starck and Ricklefs 1998). Altricial birds hatch with skeletal muscle that is less mature than precocial birds, but that grows more quickly post-hatch (Ricklefs et al. 1994). In contrast, precocial species hatch fully-feathered and are able to feed themselves (Starck and Ricklefs 1998). Because precocial species hatch at a later stage of development and, therefore, have tissue functional maturity closer to that of adults (Dietz and Ricklefs 1997; Ricklefs
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et al. 1994; Ricklefs and Webb 1985). As such, patterns of catch-up growth as well as any metabolic response to catch-up growth may differ between precocial and altricial species. We studied the sex-specific carry-over effects of food restriction and subsequent catch-up growth on the phenotype of adult Japanese quail (Coturnix japonica). Japanese quail are precocial at hatch, grow relatively rapidly (their fastest growth rate is between days 0 and 20) and are sexually mature by approximately 45 days of age (Cain and Cawley 1972). They display reverse sexual size dimorphism, with females larger than males (Cain and Cawley 1972). Importantly, because quail feed themselves shortly after hatching, the absence of parental care allowed us to isolate sex-specific effects of food restriction and catch-up growth independent of the reproductive decisions of their parents. Although there has been previous work examining food restriction in quail (Rønning et al. 2009), none, to our knowledge, has considered the carry-over effects to adulthood, nor in a sex-specific context. We hypothesized that individuals would show sex-specific sensitivity to periods of food restriction, with females (the larger sex) being more negatively affected than males (the smaller sex) at adulthood. Specifically, we predicted that females experiencing food restriction during development would be stunted in adult body size and adult body mass, and have elevated mass-specific metabolic rates at adulthood compared with control females, control males or food restricted males.
Methods Subjects Japanese quail were obtained on hatch day from Cro-Quail Farm, St. Ann’s ON, and transported to Trent University in a 37 °C incubator. Chicks were kept in a 37 °C brooder until 3 days of age, at which point they were placed in groups of 7-8 chicks in flight cages (45 cm 9 45 cm 9 90 cm) under large heat lamps with ad lib water. Temperature in cages was gradually ramped down (5 °C per week) by adjusting the heat lamps until 21 days of age, when birds were kept at 24 °C until the end of the experiment. Chicks were marked with a non-toxic coloured pen on their legs until 10 days of age, at which point they were identified with colour leg-band combinations. Birds were kept on 12:12 LD cycles and were fed MasterFeed Turkey Starter (24 % protein) from hatch to day 29. From day 29 onwards, Mazuri Adult Breeder Diet (21 % protein) was gradually introduced and Turkey Starter was phased out until birds were fed adult diet solely. Birds were maintained in groups of 7–8 per cage, and birds kept in one cage belonged to the same feeding regiment. All birds
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were group housed until day 30, when aggression prompted some individuals to be separated and singly housed. There was no difference in density of quail per cage across treatments (Chin and Burness, unpublished data). Individuals were sexed visually at adulthood with plumage, and sex was confirmed visually by inspection of gonads in a dissection post-mortem. All procedures were carried out under a Trent University Animal Care Permit (09009). Food restriction At 3 days of age, chicks were separated into four treatment groups: Control (Early ad lib/Late ad lib; AL/AL); Early Restricted (Early restricted/Late ad lib; ER/AL); Late Restricted (Early ad lib/Late restricted; AL/LR); Restricted Throughout (Early restricted/Late restricted; ER/LR). Early food restriction began on day 3 and lasted until day 13, at which point ER/AL birds were put back on ad lib food and AL/LR birds began food restriction. Late restriction began on day 13 and lasted until day 23 (the end of the rapid phase of growth). Both Late Restricted (AL/LR) and Restricted Throughout (ER/LR) were fed ad lib from day 23 until adulthood (Fig. 1). During periods of food restriction, chicks were fed between 08:00–08:30 h, 12:00–12:30 h and 16:00–16:30 h. However, due to some chick mortality in the first three replicates of the experiment, an additional feeding was added between 20:00 and 20:30 h for the last two replicates. This additional feeding did not change the amount of food given per day because the time for the 16:00 and 16:30 h feeding was split into two (yielding one 1.5-min feeding between 16:00 and 16:30 h and one 1.5 min between 20:00 and 20:30 h). All restricted chicks were fed individually. Control birds were handled daily when weighed because food restricted chicks were handled daily for feeding trials. Chicks were weighed before each feeding trial and placed into a Fig. 1 Food restriction schedule for all four treatment groups
Treatment Control (AL/AL)
feeding chamber. Chicks were then given food and allowed to feed for 3 min. After 3 min, food was taken away and chicks were then returned to group housing. Food consumption was measured in restricted birds only by weighing the food dish before feeding and after feeding. Ad lib birds had continuous access to food throughout the entire experiment, and due to group housing, it was not possible to measure food consumption in ad lib animals. The mortality rate was higher in the food restricted groups than in the ad lib group. We could not exclude the possibility that this mortality was non-random, and that weaker chicks died in the food restricted groups, but survived in the ad lib groups. Such directional selection may have resulted in higher variance in the control treatment. However, variance was homogenous in all treatments for both adult body mass (Levene’s test: F = 0.483; p = 0.695) and body size (F = 0.916; p = 0.436). This led us to conclude that even if non-random mortality occurred, its impact was relatively minor. Chicks were weighed daily until 30 days of age, at which point they were weighed every other day. Morphological measurements (exposed culmen, metatarsus, and wing chord) were taken at adulthood. Birds were raised until 50 days of age, which was considered adulthood (onset of first eggs in females) (Cain and Cawley 1972). Final sample sizes at the end of the experiment were Control (AL/AL) (n = 35; 14 females, 21 males), Early restricted (ER/AL) (n = 29; 16 females, 13 males), Late restricted (AL/LR) (n = 33; 17 females, 16 males) and Restricted throughout (ER/LR) (n = 26; 19 females, 7 males). Metabolic trials Metabolic rate at adulthood (post-hatch days 45–50) was measured indirectly as VO2 using pull-through respirometry. Birds receiving ad lib food were removed from group housing and placed in fasting chambers (single housing Food Restriction Schedule
Day:
3
50
| ----------------------------------------------------Ad libitum----------------------------------------------------|
Early (ER/AL)
3
13
Restricted
|----------Restricted---------||------------------------------------Ad libitum------------------------------------|
Late (AL/LR)
3
Restricted
|---------Ad libitum---------||---------Restricted---------||--------------------Ad libitum---------------------|
Restricted (ER/LR)
3
Throughout
|-------------------------Restricted--------------------------||-------------------Ad libitum---------------------|
13
13
50
23
23
50
50
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cages) at 16:00 h, 4 h before lights went off. Shortly before 20:00 h, each experimental bird was removed from its cage in the animal care facility, weighed (±0.01 g), placed in a breathable cloth bag and transported to the respirometry lab ca. 150 m away (\5-min travel time). Individuals were then placed into a 4 L metal metabolic chamber (1 gallon paint cans), with the inside painted flat grey, and the chamber was placed into a temperature-controlled incubator (Thermo Low Temperature Incubator, Model 915, Fisher Scientific Ltd. Nepean, ON, Canada) set 24 °C (±1 °C), which is at thermoneutrality for adult Japanese quail (Ben-Hamo et al. 2010; Freeman 1967). At 07:30 h, each individual was transported back to the animal care facility, re-weighed, and placed back in its respective cage. VO2 was measured using a pull-through flow system (Sable Systems, Las Vegas, NV) with needle valves (Luer Lock) (Lighton 2008). This set-up allowed us to measure 4 birds per trial. To measure VO2, external air was scrubbed with 3 columns of Drierite to remove water and then entered the valve multiplexer (TR-RM, Sable Systems, Las Vegas, NV, USA) and needle valves. Air then flowed into all of the chambers (each containing a bird) or into a piece of Bev-A-Line tubing (Cole-Palmer Canada, Inc., Montreal, QC, Canada) to measure baseline. Flow rate was controlled by a mass flow metre (model 840, Sierra Instruments, Amsterdam, The Netherlands) downstream from the metabolic chambers. Air exiting the chambers was then scrubbed with one column of Drierite and then was sub-sampled (TR-SS3, Sable Systems) from a 100-mL syringe barrel. Air was first drawn into a carbon dioxide analyzer (Sable Systems CA-10) and then into an oxygen analyzer (FC-10a O2 Analyzer, Sable Systems). Flow rates through the chambers were 1,800 mL/min. Each recording sequence began with measuring baseline levels for 15 min, an individual bird for 25 min, and then another 15 min of baseline. The system would then automatically switch to begin recording O2 in the next chamber. This set-up allowed for collection of at least 125 min of O2 measurements from each bird over the course of the 12-h night. Data were collected with the Warthog data collection program and analyzed with Warthog Lab Analyst (Warthog system, www.warthog.ucr.edu). As an index of resting metabolic rate (RMR), we estimated the minimum VO2 for each individual by identifying the lowest 5 min of continuous oxygen consumption per night, and using equation 11.7 from Lighton (2008). Dissection of muscle tissue One week after respirometry, birds were euthanized (ca. 50 days old) with an overdose of sodium penobarbital (Euthanasol) and rapidly dissected. The left pectoralis major and supracoracoideous (SC) muscle were removed and
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weighed to obtain a wet tissue weight. Muscle tissues were then frozen at -20 °C, then moved to -80 °C overnight prior to placing on the freeze drier. Muscle tissues were freeze dried to a constant mass (2–3 days), and were then reweighed to obtain a dry weight. After grinding with a mortar and pestle, a sub-sample of each muscle (1 g ± 0.10 g) was then weighed and placed into a small filter paper envelope for lipid extraction. Muscle samples were fat-extracted in a Soxhlet Apparatus (Fisher Scientific) for 6 h using petroleum ether as a solvent, air-dried overnight, and then subsequently oven-dried at 60 °C for a further 24 h. Following oven-drying, muscle samples were cooled overnight in a desiccator, and then re-weighed. Lipid-free dry mass was then used to calculate water content of the tissue. Water content was calculated as per Ricklefs and Webb (1985). Statistics The effects of treatment (early restriction; late restriction; early and late food restriction; and ad lib food) and sex on juvenile body mass, adult body mass, and adult RMR were analyzed using general linear mixed models at each age range with planned Tukey’s HSD post hoc tests between control (AL/AL) and restricted birds. Because there were only two treatments during early food restriction (days 3 to 13), birds were grouped into ad lib (AL/AL and AL/LR) or restricted (ER/AL and ER/LR) for analyses between days 3 to 13. Initial body mass (day 3 body mass) was included as a covariate for all juvenile body mass analyses. For adult RMR, body mass (average of pre- and post-metabolism trial) was included as a covariate and chamber number was included as a cofactor. In no analysis was chamber number significant (all p [ 0.05). The treatment x sex interaction term was included in all models, and was eliminated if nonsignificant. Experimental replicate number was included in all models as a cofactor. Approximately 25–30 individuals were included in each replicate, as the experiment was replicated 5 times. Food consumption during each day of food restriction from days 3 to 23 was analyzed with general linear mixed models at each age and each treatment with sex as a fixed factor. Experimental replicate number was included in all models as a cofactor. Body mass was added as a covariate. The effects of sex and treatment on body size and body mass at adulthood were analyzed using general linear mixed models with experimental replicate as cofactor and Tukey’s LSD post hoc tests if necessary. When testing the effect of sex and treatment on body size at adulthood using a general linear mixed model, we generated a principal components score (PC1) based on the covariance matrix of log 10 transformed culmen, tarsus, and wing cord at 50 days of age. The traits loaded positively, and PC1 had an eigenvalue of 0.0009 and explained 61.5 % of variation.
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One individual with a high student residual ([2.5) was excluded from the analysis of adult body mass, while a single individual with a low student residual (\-2.5) was excluded from the analyses of adult body size. The effects of treatment and sex on muscle water content and dry muscle mass were analyzed using general linear mixed models. The covariate (body mass - muscle water content) was included in the models analyzing water content of muscles, and (body mass - dry muscle mass] was the covariate in the models analyzing dry muscle mass. These covariates were designed to avoid the problems of part-whole correlation (Christians 1999). Experimental replicate was added as an additional effect. Treatment 9 sex interaction terms were included in all models and were eliminated if non-significant. All tests were two-tailed, with statistical significance set at p \ 0.05, and were conducted using PASW Statistics 19, Release Version 19.0.0 (O SPSS Inc., 2010. Chicago, IL, www.spss.com). All results are presented as least squares mean ± standard error of the mean.
Results Effect of food restriction and re-feeding on juvenile body mass Juvenile body masses on days 3, 13, 23 and 33 are depicted in Fig. 2. At the beginning of food restriction (day 3), restricted (ER/LR and ER/AL) birds were heavier than ad lib (AL/AL and AL/LR) birds (F1,115 = 27.04; p \ 0.001) (Fig. 2a).
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Although significant, this difference was presumably due to random chance, and given the directionality, was unlikely to affect our conclusions. There was no sex difference in body mass at the beginning of food restriction (F1,115 = 0.072; p = 0.789). By the end of early food restriction (day 13), restricted birds (ER/LR and ER/AL) were significantly lighter than ad lib (AL/AL and AL/LR) birds (F1,114 = 728.86; p \ 0.001) (covariate day 3 mass: F1,114 = 47.08; p \ 0.001) (Fig. 2b). There also was no overall sex difference in body mass at day 13 (F1,114 = 1.10; p = 0.297). At the end of late food restriction, there was a significant effect of treatment on day 23 body mass (F3,112 = 252.12; p \ 0.001)(covariate day 3 mass: F1,112 = 39.96; p \ 0.001), with ad lib birds (AL/AL) being heavier than any other treatment group, despite 10 days of re-feeding in ER/ AL chicks (Fig. 2c). There was again no sex difference in body mass at day 23 (F1,112 = 1.85 l; p = 0.176). 10 days after late food restriction ended, there was still a significant effect of treatment on body mass (F3,109 = 45.11; p \ 0.001)(covariate day 3 mass: F1,112 = 40.63; p \ 0.0001) (Fig. 2d), with ad lib birds still heavier than any other treatment group, despite 20 days of re-feeding in ER/AL chicks, and 10 days of re-feeding in ER/LR and AL/LR chicks. There was a sex difference in body mass at day 33, with females heavier than males (F1,112 = 7.094; p = 0.009). When examining mass change over 10 day intervals, ad lib birds gained approximately 7 times more mass between days 3 and 13 (early restriction) than did restricted birds (F1,115 = 642.68; p \ 0.0001) (Fig. 3a). There was no sex difference in mass gained during days 3–13 (F1,115 = 1.15;
Fig. 2 Mass of juvenile Japanese quail at a day 3, b day 13, c day 23 and d day 33 posthatch. Significant differences between control and restricted groups are denoted by differing letters. All values are expressed as least squared means ± standard error of the mean (controlling for sex); however, error bars were small and were generally hidden by symbols
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Fig. 3 Average mass change in juvenile Japanese quail calculated over 10-day intervals: a days 3–13, b days 13–23, c days 23–33 and d days 33–50. Significant differences between control and restricted groups are denoted by differing letters. All values are expressed as least squared means ± standard error of the mean (controlling for sex); however, error bars were small and were generally hidden by symbols
p = 0.287). Between days 13 and 23, there was a significant treatment effect on mass gained (F3,113 = 307.94; p \ 0.001), with late restricted (AL/LR) birds losing mass, and birds restricted throughout development (ER/LR) gaining little mass compared to control (AL/AL) (both p \ 0.001) (Fig. 3b). Early restricted (ER/AL) birds did not differ in mass gain from control between days 13 and 23 (p = 0.706). Females gained more mass than males between days 13 and 23 (F1,113 = 4.71; p = 0.032). Between days 23 and 33 (Fig. 3c), there was still a significant effect of treatment on mass change (F3,113 = 114.05; p \ 0.001). All three restricted groups gained significantly more mass than control birds (all p \ 0.001) (Fig. 3c). Females gained more mass than males between days 23 and 33 (F1,113 = 6.94; p = 0.01). Finally, between days 33 and adulthood, there was a significant treatment effect on mass change (F3,113 = 27.25; p \ 0.001), with all restricted groups still gaining more mass than control birds (all p \ 0.05) (Fig. 3d). There was no significant sex difference in mass change at this age range (F1,113 = 2.73; p = 0.10). Food consumption was measured at all days of restriction from days 3 to 23. At no point was there a sex difference in food consumption (all p [ 0.05). Due to group housing, food consumption was not measured in ad lib birds. Effects of food restriction and re-feeding on adult phenotype In adults, there was an overall treatment effect on body mass (F3,120 = 4.80; p = 0.0035). Both early restricted
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(ER/AL) and restricted throughout development (ER/LR) birds were significantly lighter than control (AL/AL) (planned post hoc, both p \ 0.05). Individuals subjected to late restriction only (AL/LR) did not differ from controls (p [ 0.05), suggesting that only early food restriction (but not late restriction) had a long-term effect on adult body mass (Fig. 4a). Overall, females were heavier than males (F1,122 = 12.10; p = 0.007). There was no significant treatment 9 sex interaction term (p [ 0.05). There was no overall difference between restricted birds and control birds in body size (PC1 scores) at adulthood (F3,121 = 1.59; p = 0.195), nor did males and females differ in adult body size (F1,121 = 3.46; p = 0.07). However, the effect of food restriction on adult body size differed between males and females (treatment 9 sex: F3,121 = 2.95; p = 0.04). In Control birds (AL/AL), females were larger than males (F1,27 = 5.02; p = 0.033). However, females and males were of equal size in early restricted (ER/AL) (F1,23 = 1.13; p = 0.298), late restricted (AL/LR) (F1,27 = 0.645; p = 0.429) and birds restricted throughout development (ER/LR) (F1,21 = 0.126; p = 0.726) (Fig. 4b). At adulthood, there was no difference in metabolic rate (oxygen consumption) among treatment groups (F3,55 = 0.91; p = 0.45; Body Mass F1,55 = 6.66; p = 0.0003) (Fig. 4c), indicating that food restriction and subsequent catch-up growth has no long-term effects on metabolic rate. Males had higher metabolic rates than females, but this failed to attain significance (F1,57 = 3.16; p = 0.08; Body mass: F1,57 = 15.44; p = 0.0003).
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p = 0.983; covariate: [body mass - supracoracoideus dry mass], p \ 0.001). There was also no overall effect of treatment on water content of muscles (pectoralis major— covariate: [body mass - pectoralis water content], p \ 0.001; supracoracoideus—covariate: [body mass - supracoracoideus water content], p \ 0.001) (Table 1), suggesting that birds had also caught up in functional maturity in both muscles tissues by adulthood. There was no sex difference in water content of either muscle tissue at adulthood (pectoralis major: F1,92 = 0.13; p = 0.722; covariate: [body mass - pectoralis water content], p \ 0.001; supracoracoideus: F1,92 = 0.015; p = 0.902; covariate: [body mass supracoracoideus water content], p \ 0.001).
Discussion In this study, we demonstrated that food restriction and catch-up growth had few long-term effects on adult phenotype. Early, but not late, food restriction during development negatively affected Japanese quail adults. Although individuals undergoing early food restriction attained similar structural size as individuals fed ad lib, they were lighter as adults, and thus in poorer condition. As predicted, males and female differed in their sensitivity to environmental conditions during development. Females had larger body size than males when both were fed ad lib, however, under conditions of food restriction females and males no longer differed in size, indicating that females are more sensitive than males to reductions in environmental quality. There was no difference in adult metabolic rate between food restricted and control individuals, suggesting that Japanese quail do not pay the metabolic cost to catch-up growth as previously suggested for altricial species (e.g., zebra finches: Criscuolo et al. 2008; song sparrows: Schmidt et al. 2012). Fig. 4 Adult a body mass; b body size and c resting metabolic rate in male and female Japanese quail at day 50. Adult body size is expressed as the first principle component (PC1) calculated from log10(culmen), log10(tarsus) and log10(wing cord). Resting metabolic rate is expressed as oxygen consumption in mL/h with body mass as a covariate. Significant differences between control and restricted groups are denoted by differing letters. The asterisk in (b) denotes a significant sex-effect within the control treatment. All values are expressed as least squared means ± standard error of the mean
There was no effect of treatment on dry mass of either breast muscle (pectoralis major: covariate: [body mass - pectoralis dry mass], p \ 0.001; supracoracoideus: covariate: [body mass - supracoracoideus dry mass], p \ 0.001) (Table 1), suggesting that restricted birds had caught up in muscle size by adulthood. There was no sex difference in dry mass in either muscle (pectoralis major: F1,92 = 0.0001; p = 0.998; covariate: [body mass - dry pectoral mass], p \ 0.001; supracoracoideus: F1,92 = 0.004;
Growth rate Japanese quail demonstrated catch-up growth following both early and late food restriction. Catch-up growth has been previously demonstrated in birds (Arnold et al. 2007; Criscuolo et al. 2008; Hegyi and Torok 2007; Honarmand et al. 2010), including Japanese quail (Ocak and Erener 2005; Schew and Ricklefs 1998), which was in part why we chose quail as a model species. However, catch-up growth previously demonstrated in altricial species was the result of varying levels of protein in the diet (Arnold et al. 2007; Criscuolo et al. 2008; Honarmand et al. 2010) rather than total energy intake. Varying energy intake has typically been examined via brood manipulation (Burness et al. 2000; Verhulst et al. 2006) or decreasing parental care (Hegyi and Torok 2007; Velando 2002). Varying
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Table 1 Dry mass and water content of left pectoral and left supracoricoideus muscles in 50-day-old adult Japanese quail raised on different food restriction schedules Muscle
Treatment AL/AL
Pectoralis major dry weight (g) Water content (g) Supracoricoideus dry weight (g) Water content (g)
Statistics ER/AL
AL/LR
ER/LR
F
p
4.30 ± 0.11
4.45 ± 0.12
4.45 ± 0.13
4.53 ± 0.14
0.688
0.562
11.34 ± 0.34
11.91 ± 0.36
11.69 ± 0.39
12.15 ± 0.42
1.24
0.298
1.43 ± 0.05 4.03 ± 0.14
1.48 ± 0.05 4.27 ± 0.15
1.50 ± 0.06 4.34 ± 0.16
1.41 ± 0.06 4.02 ± 0.18
0.277 0.331
0.842 0.803
Degrees of freedom was 3, 92 for each tissue. Water content, an index of muscle maturity, was calculated following Ricklefs and Webb (1985) All values are least squared means ± standard error of the mean. No sex difference was detected in any tissues AL/AL (Control) ad lib, ER/AL early restriction, AL/LR late restriction, ER/LR restricted throughout development
levels of protein may have very different physiological effects from food restriction. For example, food restriction results in the reduction in size of various alimentary organs (Brze˛k et al. 2009; Burness et al. 2000; Killpack and Karasov 2012), while protein restriction results in an increase in protein transporters in the intestine (Gilbert et al. 2008). Reducing alimentary organ size may serve to conserve limited energy (Killpack and Karasov 2012), whereas elevating protein transporters can maximize uptake of limited resources. Catch-up growth following food restriction may allow underfed individuals to catch up to the appropriate adult size. However, previous studies suggest that food restricted birds that are re-fed demonstrate both positive and negative changes in physiology and behaviour at adulthood. For example, zebra finches suffer delayed onset to breeding, decreased rate of egg production (Birkhead et al. 1999; Blount et al. 2006; Metcalfe and Monaghan 2001), and a decline in flight performance post-breeding (Criscuolo et al. 2011). In contrast, zebra finches that experienced low protein diets and subsequently underwent catch-up growth were quicker to engage in foraging (Krause et al. 2010) and exploratory behaviour (Krause and Naguib 2011). However, if costs to catch-up growth following re-feeding are too large, it may be beneficial to remain small at adulthood rather than undergo catch-up growth. Moreover, it is important to note that food restriction and catch-up growth were always coupled in both this study and previous studies, and it is not possible to attribute these costs solely to either food restriction or catch-up growth. Because we did not follow quail for the duration of their lives, it is unclear what physiological or behavioural changes adult quail may incur later in life due to food restriction and subsequent re-feeding. Effect of juvenile environmental conditions on adult phenotype Adult body mass, but not body size, was significantly higher in control groups (AL/AL and AL/LR) compared to
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animals that had experienced early food restriction (ER/AL and ER/LR). This suggests that the specific time during development in which food restriction occurs, rather than the length of time an individual undergoes catch-up growth, may be more important on determining the adult phenotype. Moreover, this also suggests that birds that experience food restriction later during development, and at a larger size, are able to catch up to the appropriate adult mass. Because late restricted (AL/LR) individuals were heavier when they initially underwent food restriction (compared to early restricted individuals), they did not have as much mass to gain upon re-feeding. Additionally, early food restriction may encompass specific developmental phases in Japanese quail that may be vulnerable to food restriction (reviewed in Schew and Ricklefs 1998). This may contribute to the differences in body mass between birds that underwent early food restriction and those that did not. Previous studies that have manipulated protein content early in development have produced mixed results. There were no differences in adult body mass between female zebra finches that had diets of differing protein content during development (Krause et al. 2010). However, the diet of these zebra finches was switched partway through development (i.e. individuals did not have the same protein content diet throughout development). In contrast, zebra finches (of both sexes) raised on a high-quality, protein supplemented diet were heavier as adults than zebra finches raised on a seed-only diet (Bech et al. 2004), but these individuals did not switch diets during development. Because we did not follow individual quail for the duration of their natural lives, it is unknown if birds that were food restricted early in development would have attained similar adult body mass to control birds had they been allowed to grow longer. However, results from another study in our research group suggest that although individual quail continue to gain mass beyond 50 days of age, the mass differences resulting from early rearing environments are still present when individuals are over 120 days of age (Burness et al. unpublished data).
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We detected a sex difference in adult body size in control birds, but not in food restricted birds. This suggests that the structural size of females may be more sensitive than that of males to reductions in environmental quality. Sex-specific sensitivity to developmental environment has been seen in other animals displaying reverse sexual size dimorphism (Fargallo et al. 2002; Hipkiss et al. 2002; Laaksonen et al. 2005; Torres and Drummond 1997). The larger sex may be more sensitive to fluctuating resources in the environment as they may require more resources to develop (Anderson et al. 1993). However, unlike previous studies, our study was independent of parental control— that is, parental investment did not contribute to resource availability. If during development female quail typically require more food per day than do males, then the food restriction regime we employed may have been more severe for females than for males (because both males and females of the same treatment were allowed access to food for the same duration). If this were the case, this may help explain why females appeared more sensitive than males to undernutrition (with respect to body size). Although we could show that food consumption did not differ between males and females during food restriction, we were unable to measure food intake in ad lib birds (because they were initially group housed). As such, we do not know if there was a sex difference in food intake during re-feeding or in control birds throughout development. This is a challenge associated with many studies assessing sex-specific sensitivity, particularly those of species requiring group housing (e.g., quail), or in which there is more than one nestling in a brood (e.g., zebra finches). There was no treatment difference in functional maturity (measured as water content in grams) or dry mass of muscle tissues. In the few studies to consider the effect of catch-up growth and early food restriction in altricial birds, internal organs had achieved the appropriate adult size by the time of fledging (Brze˛k and Konarzewski 2004; Burness et al. 2000), despite the fact that internal organs are reduced during times of food restriction to save energy (Killpack and Karasov 2012). This implies that timing of food restriction does not affect pectoralis and supracoracoideus muscle tissue, suggesting that a poor early developmental environment does not hinder the capacity for flight. Moreover, the difference in adult body mass between control birds and birds that underwent early food restriction cannot be attributed to differences in muscle mass or maturity. Additionally, precocial birds such as Japanese quail have higher developmental flexibility than do altricial birds (reviewed in Schew and Ricklefs 1998). For example, chickens that underwent food restriction early in development (1 week) resumed typical growth and maturation rates for their age, and subsequently reached
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adult mass and morphology (Gordon 1960). Turkey toms that were protein restricted during development did not differ in bone length or composition at 18 weeks of age (Turner and Lilburn 1992). This developmental flexibility may also play a role in the lack of differences in muscle mass at adulthood. There was no carryover effect of food restriction or catch-up growth during development on adult RMR, in contrast to previous work on zebra finches (Criscuolo et al. 2008; Verhulst et al. 2006). That is, metabolic rate was not elevated in adult quail, regardless of timing or duration of food restriction. Although studies have suggested an energetic cost associated with catch-up growth (Criscuolo et al. 2008; Verhulst et al. 2006), this effect was not seen in adult Japanese quail. As with muscle tissue, this lack of difference in metabolic rate may be due to the developmental flexibility of precocial Japanese quail (Schew and Ricklefs 1998). Additionally, the detected metabolic cost in altricial species depended on experimental protocol and sex of offspring. For example, Criscuolo et al. (2008) manipulated protein content of diet during development. Bech et al. (2004) also manipulated protein content in the diet, but did not detect an effect on adult BMR (Bech et al. 2004). In contrast, Verhulst et al. (2006) manipulated total resource availability via brood manipulation. In their study, female zebra finches in enlarged broods had higher metabolic rates compared to females in smaller broods, but this effect was not present in males (Verhulst et al. 2006). Our findings suggest that regardless of timing or duration of food restriction, there was no effect of catch-up growth on the metabolic rate of adult Japanese quail.
Conclusions This study examined possible sex differences in environmental sensitivity in a precocial species, and whether these sex-specific effects carried over into adulthood. We tested whether food restriction followed by catch-up growth affected adult body mass and size, and whether costs of catch-up growth were manifested in adults as an increased metabolic rate, as previously reported in altricial zebra finches. While we demonstrated that Japanese quail can accelerate growth rate following re-feeding, restriction early in development appears to affect adult body mass. Moreover, females appear to be more sensitive to developmental environment, as control females were larger than control males, but restricted birds showed no sex difference in adult body size. There were no differences among treatments in metabolic rate at adulthood, suggesting no carry-over effect of catch-up growth on energy expenditure. Future studies should test whether developmental stressors, such as food restriction and/or catch-up growth,
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have carry-over effects in the form of elevated stress responsiveness in adults. Acknowledgments We wish to thank L. Jones, J. Sparks, H. Koslowsky and J. Huard for help with feeding trials and measurements. We also wish to thank T. Luloff for advice and help with statistical analyses. This research was funded by grants from the Natural Sciences and Engineering Research Council (NSERC), the Canadian Foundation for Innovation and the Ontario Innovation Trust to G.B., an NSERC Post-graduate Scholarship to E.HC., and NSERCUndergraduate Student Research Award to R.J.K.
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