Environmental influences on the evolution of growth and developmental rates in passerines

Abstract.— The reasons why growth and developmental rates vary widely among species have remained unclear. Previous examinations of possible environmental influences on growth rates of birds yielded few correlations, leading to suggestions that young may be growing at maximum rates allowed within physiological constraints. However, estimations of growth rates can be confounded by variation in relative developmental stage at fledging. Here, we re-estimate growth rates to control for developmental stage. We used these data to examine the potential covariation of growth and development with environmental variation across a sample of 115 North American passerines. Contrary to previous results, we found that growth rates of altricial nestlings were strongly positively correlated to daily nest predation rates, even after controlling for adult body mass and phylogeny. In addition, nestlings of species under stronger predation pressure remained in the nest for a shorter period, and they left the nest at lower body mass relative to adult body mass. Thus, nestlings both grew faster and left the nest at an earlier developmental stage in species with higher risk of predation. Growth patterns were also related to food, clutch size, and latitude. These results support a view that growth and developmental rates of altricial nestlings are strongly influenced by the environmental conditions experienced by species, and they generally lend support to an adaptive view of interspecific variation in growth and developmental rates.     

Effects of food shortage and oversupply on energy utilization, histology, and function of the gut in nestling song thrushes (Turdus philomelos)

We measured food intake, digestive efficiency, body mass increments, resting metabolic rate (RMR), carcass fat content, size and histological structure of the gut, and the rate of intestinal brush border uptake of l-proline in song thrush (Turdus philomelos) nestlings subjected to food shortage or food surplus under laboratory conditions. We assigned nestlings between 3 and 7 d of age to one of the following treatments: (1) food restriction, which resulted in a slowed growth at the rate found in undernourished, wild nestlings; (2) overfeeding, which totally suppressed begging; and (3) intermediate feeding. Threefold differences in energy consumption caused fivefold differences in body mass increments of the nestlings. Despite this, body mass-corrected RMR and intestinal mass were not affected by the feeding regime. The energy content of fecal output was highest in food-restricted birds, while their carcass fat content was lowest among treatment groups. Intestinal uptake rates of l-proline were low in the overfed and intermediate-fed young but significantly increased in the food-restricted birds, who attempted to maximize their rates of growth and development within the restrictive limits set by feeding regime. We noted a marked decrease of intestinal villi height in overfed birds as compared to intermediate-fed and food-restricted nestlings. We conclude that song thrush nestlings are characterized by a limited plasticity of their developmental program, which prohibits overfed nestlings from significantly up-regulating their gut function to accommodate increased food intake. This suggests that they already grew at a rate close to their physiological maximum. We suggest two interpretations: (1) under natural conditions, song thrush nestlings do not face frequent, unpredictable fluctuations in food abundance that could select for developmental plasticity, or (2) strong selection for uniform adult phenotypes prevents flexible developmental trajectories, which would result in a diversity of adult phenotypes.     

The effect of food restriction on morphological and metabolic development in two lines of growing Japanese quail chicks

To investigate whether there is a relationship between the inherent maximum growth rate of a chick and its degree of developmental plasticity, we studied the effects of food restriction on morphological and physiological development in P-line (selected for high growth rates) and C-line (nonselected) chicks of the Japanese quail between 2 and 64 d of age. In each line, three groups were created; one group in which the chicks were fed ad lib. and two other groups in which the chicks received 70% and 40% of the line-specific ad lib. feeding levels, respectively. In all three groups, chick survival rates were very high, and no relationship was detected between feeding level and chick mortality. The experimental feeding levels strongly affected the chicks' attainment of body mass at all ages. In addition, at most ages the growth of the structural components (wing, tarsus, and head) were also significantly affected by the feeding experiment but to a much smaller extent than the body mass. The feeding levels also affected the achievement of female sexual maturity such that, at the end of the experiment, most of the ad lib.-fed females and none of the females that received 40% of the ad lib. feeding level were laying eggs. In chicks of both lines that were fed ad lib., homeothermy was achieved at 7 d of age, but in chicks that received 40% of the line-specific ad lib. levels, homeothermy was achieved after 15-22 d of age. Poikilothermic chicks (P- and C-line) that were relatively heavy for their age exhibited relatively high resting metabolic rates (RMRs) and peak metabolic rates (PMRs) for their age. In addition, a positive relationship was found between the chicks' relative mass and RMR (based on mass-based predictive equations). No relationship was detected between the chicks' relative body mass and their relative PMR (relative to mass-based predictive equations). With respect to the metabolic scope (i.e., PMR-RMR), Japanese quail chicks exhibited remarkable developmental plasticity: chicks with body masses that were 50% lower than the normal growing chicks did exhibit a normal capacity of thermogenic heat production for their mass. Because no differences were found with respect to the level of plasticity of morphological and physiological development between the two strains, we conclude that the selection for high postnatal growth rates in P-strain chicks has not resulted in a in a higher vulnerability of these chicks to food restrictions.     

Influence of hatching order on growth rate and resting metabolism of kestrel nestlings

Hatching asynchrony in altricial birds may result in a competitive disadvantage for the youngest nestlings compared to older siblings. We studied the effects of a size hierarchy on the growth rate of Eurasian kestrels Falco tinnunculus chicks in nests with and without access to supplemented food in western Finland. Body mass stopped increasing on the 19th day after hatching while body size, estimated by a combination of bone and feather lengths continued to increase at least until fledging at 26 days. Body condition, reflecting muscle and fat, did not change markedly during the growth period from the 12th day to fledging. Body temperature and resting metabolism were usually lower in nestlings 12 days old than in nestlings at fledging. Growth of body mass, size and condition, and resting metabolism were delayed in last-hatched nestlings aged 19 days. Just before fledging, last-hatched nestlings attained a similar body mass and size, and had a similar resting metabolism to those of older siblings. At fledging, only in nests without access to supplemented food was the body condition of last-hatched chicks lower than that of its siblings, but in nests with access to supplemented food no such difference was detected. Our results highlight that the level of lipids in the last-hatched nestling can be affected by the food restriction imposed by hatching order.     

Sex-specific development of cell-mediated immunity under experimentally altered rearing conditions in blue tit nestlings

In birds, poor rearing conditions usually have negative effects on T-cell-mediated immune response. However, earlier studies demonstrate that fitness-related traits such as body mass may show sex-specific patterns when subject to alteration of rearing conditions. Therefore, to investigate whether deterioration of rearing conditions influences the development of immune function differently in male and female nestlings, we performed brood size manipulation experiments on blue tit (Parus caeruleus) nestlings. To alter rearing conditions, some broods were increased by three nestlings soon after hatching, while other broods were left non-manipulated. Immune response was assessed as a hypersensitivity reaction to phytohaemagglutinin in 11-day-old nestlings. Additionally, we studied the consequences of brood size manipulation for fledgling body mass and tarsus length. The enlargement of brood size had different effects on the cellular immune responses of male and female nestlings, with males being more negatively affected than their female nest-mates. Sex-specific effects of poor rearing conditions were also recorded for tarsus length, such that tarsus growth was more retarded in female than in male nestlings. We discuss the effects of deterioration of rearing conditions on sex-specific development of cell-mediated immunity with respect to sexual dimorphism of size and developmental strategies in male and female nestlings.     

Developmental plasticity in a passerine bird: an experiment with collared flycatchers Ficedula albicollis

Young birds often face poor food supply, which reduces their growth and development. However, if the shortage of resources is only temporary, there is a possibility to adjust the growth trajectory of morphological traits after the end of the short-term limitation period. The two main ways of compensatory growth are delayed development (parallel growth) and growth acceleration (catch-up growth). Parallel growth has been widely demonstrated in birds, but the presence of catch-up growth in altricial species has been questioned. However, most experiments have been conducted in laboratory conditions. We manipulated the food supply of nestling collared flycatchers Ficedula albicollis in the wild by removing the male parent for three days at 4–7 days of chick age. We performed early partial swapping to control for origin effects on growth, and total swapping after the period of food limitation to ensure similar late growth environment for deprived and control chicks. Both body mass and tarsus length of deprived chicks was negatively affected by the food scarcity. Body mass showed efficient catch-up growth, but this compensation was absent in skeletal size. Body mass is an important determinant of postfledging survival in this long-distance migrant. Further studies are needed in a variety of species to examine developmental plasticity in relation to age at food scarcity and the allocation hierarchy of various morphological traits.     

Sex differences in compensatory and catch-up growth in the mosquitofish Gambusia holbrooki

In many taxa, temporary nutritional shortage early in development can favour compensatory strategies that include elevated growth (‘compensatory growth’) and/or extension of the usual period of development (‘catch-up growth’) once conditions improve. The net gains from each strategy depend on the extent to which larger body size increases fitness relative to associated costs (e.g. long-term effects on adult performance, or a greater risk of juvenile mortality). These costs and benefits are likely to differ between the sexes due to sex-specific selection. We documented the responses of male and female mosquitofish (Gambusia holbrooki) to 3 weeks of low food availability (7–28 days old) that restricted subsequent growth and morphology compared to control fish continuously reared on a high food diet (N = 635 fish total). Neither sex elevated their growth rate immediately after being returned to a normal diet compared to control fish. When measured over the entire period until maturation, however, females showed compensatory growth. Males did not. Both sexes also exhibited catch-up growth but the delay until maturation was significantly longer for males. Despite early growth restriction, both sexes eventually matured at almost the same size as control fish, although males had a significantly smaller gonopodium (a sexually selected trait) than that of control males. Reasons for these sex differences are discussed.     

Sex and environmental sensitivity in blue tit nestlings

In birds and mammals with sexual size dimorphism (SSD), the larger sex is typically more sensitive to adverse environmental conditions, such as food shortage, during ontogeny. However, some recent studies of altricial birds have found that the larger sex is less sensitive, apparently because large size renders an advantage in sibling competition. Still, this effect is not an inevitable outcome of sibling competition, because several studies of other species of altricial birds have found the traditional pattern. We investigated if the sexes differ in environmental sensitivity during ontogeny in the blue tit, a small altricial bird with c. 6% SSD in body mass (males larger than females). We performed a cross-fostering and brood size manipulation experiment during 2 years to investigate if the sexes were differently affected as regards body size (body mass, tarsus and wing length on day 14 after hatching) and pre-fledging survival. We also investigated if the relationship between body size and post-fledging survival differed between the sexes. Pre-fledging mortality was higher in enlarged than in reduced broods, representing poor and good environments, respectively, but the brood size manipulation did not affect the mortality rate of males and females differently. In both years, both males and females were smaller on day 14 after hatching in enlarged as compared to reduced broods. In one of the years, we also found significant Sex × Experiment interactions for body size, such that females were more affected by poor environmental conditions than that of males. Body size was positively correlated with post-fledging survival, but we found no interactive effects of sex and morphological traits on survival. We conclude that in the blue tit, females (the smaller sex) are more sensitive to adverse environmental conditions which, in our study, was manifest in terms of fledgling size. A review of published studies of sex differences in environmental sensitivity in sexually size-dimorphic altricial birds suggests that the smaller sex is more sensitive than the larger sex in species with large brood size and vice versa.     

Lack of compensatory body growth in a high performance moose Alces alces population

Considerable work has been done on disentangling important factors determining early development in body size, yet our knowledge of the extent to which animals living under varying conditions can achieve catch-up growth for a bad start in life is limited. Here, we investigated how body mass at the age of 8 months influenced adult body mass in a moose Alces alces population living under excellent environmental conditions on the island of Vega in northern Norway. We also investigated if mother age and birth date effects on calf body mass persisted until adulthood. We show that neither males nor females were able to show compensatory growth before they reached adulthood, and that part of the variation in adult body mass may have been due to variation in mother age and date of birth. The pattern observed in males can be related to their growth strategy in relation to reproduction, while such results were not expected in females where size-dependent start of reproduction is likely to interact with body growth. We suggest that the good environmental conditions experienced on Vega led to females having small somatic costs of an early start of reproduction or that larger females were able to acquire more resources for growth than their smaller conspecifics. In both cases, females that postpone their first reproduction may not be able to achieve catch-up growth for their lower early body mass compared to females that start reproduction at an early age. Our results concur with previous studies indicating that compensatory growth is weak in moose, increasing the likelihood that variation in life history characters are also transferred between generations.     

Effects of ectoparasites of young on parents' behaviour in a Mediterranean population of Blue Tits

In altricial birds, adults are expected to alleviate the impact of parasitism on their young by increasing parental care. We experimentally investigated the effects of blowfly parasitism on adult behaviour in the nest cavity in a population of Blue Tits in which nestlings are heavily parasitized by blowfly larvae. The behaviour of males and females was different, since only the females carried out nest sanitation activities related to the presence of parasites. The time females devoted to nest sanitation was higher in parasitized nests than in experimentally deparasitized ones, suggesting that chicks and adults might share the costs of blowfly parasitism.     

Body weight,energy metabolism,and time in the life of birds

The breeding of birds, both large and small, is affected by two specific factors: (1) hypometry of egg weight relative to female body weight and (2) seasonality of breeding, with the favorable period being limited and almost equal for birds of different body sizes. Dozens of published allometric formulas describing the dependence of energy parameters of eggs and nestlings at different growth stages and the energy cost of parental care on the body weight of parents, eggs, and nestlings, respectively, are reviewed. It is shown that birds, especially species with a large body weight, repeatedly change their metabolic parameters during ontogeny in order to shorten the period of breeding and growth. In most species, the energy costs of breeding in both sexes are approximately equal. Bringing food in the bill allows birds to supply nestlings with the amount of energy that is dozens of times greater than that expended for obtaining the food. In placental mammals, only females are involved in offspring development. Therefore, the growth rate of embryos and energy expenditures for milk feeding are limited by the metabolic potential of the mother. As a consequence, mammalian offspring grow ten times slower than bird nestlings, the body weights of females being equal.     

Two sexes respond equally to food restriction in a sexually dimorphic but not body mass dimorphic jumping spider

Natural selection favors animals that evolve developmental and behavioral responses that buffer the negative effects of food restrictions. These buffering responses vary both between species and within species. Many studies have shown sex‐specific responses to environmental changes, usually in species with sexual size dimorphism (SSD), less found in species with weak or no SSD, which suggests that sizes of different sexes are experiencing different selections. However, previous studies usually investigated development and behavior separately, and the balanced situation where males and females of sexually dimorphic species respond in the same way to food restriction remains little known. Here, we investigated this in Phintelloides versicolor (Salticidae) that presents sexual dimorphism in color and shape but weak SSD. We examined whether food restriction induced the same responses in males and females in development duration, adult body size and weight, daily time allocated to foraging, and hunting. We found food restriction induced similar responses in both sexes: both exhibited longer development duration, smaller adult body size and weight, higher probability of staying outside nests and noticing prey immediately, and higher hunting success. However, there were sexual differences regardless of food condition: females showed faster development, smaller adult body size, higher probability of staying outside of nests, and higher hunting success. These indicated the differential selection on male and female sizes of P. versicolor could be under a balanced situation, where males and females show equal developmental and behavioral plasticity to environmental constraints.     

Sex-specific life history patterns in bluegill (Lepomis macrochirus): interacting mechanisms influence individual body size

The ultimate body size that an individual fish achieves can be a function both of direct effects of growth or indirect effects associated with the timing of sexual maturation (and associated energetic tradeoffs). These alternatives are often invoked to explain variation in body size within and among fish populations, but have rarely been considered simultaneously. We assessed how resource availability and timing of maturation interact to influence individual body size of bluegill (Lepomis macrochirus). Resource availability (high and low food) and the social structure of the population (presence or absence of large, mature males) were varied in experimental ponds. Food ration affected growth (larger fish in the high food treatments) and the social structure of the population affected timing of maturation (early maturation of males in the absence of large males). Treatment effects, however, were sex-specific; males responded to the social structure of the population and females were more responsive to resource availability. We also found individuals that became sexually mature were smaller than those that remained immature, although results were sex-specific and resource dependent. For males, individuals that matured were smaller when resources were limited; mature and immature females showed no difference in body size regardless of food ration. We show that both resource availability and the processes that control timing of maturation interact in sex-specific ways to influence body size of bluegill. These results suggest that a more robust explanation for variable body size requires consideration of sex-specific interactions between ecological (food and growth) and evolutionary (timing of maturation) mechanisms.     

Cardiomyocyte ploidy levels in birds with different growth rates

Cytofluorimetric study of ploidy levels in ventricular cardiomyocytes was carried out on 36 adult bird species belonging to 10 orders as well as on the quail Coturnix coturnix, of different ages. It was shown that polyploidization of quail cardiomyocytes occurs during the first 40 days after hatching and ends by the time growth is completed. In adult birds, the cardiomyocyte ploidy hardly changed at all. Interspecies comparison revealed that in the adult bird myocardium 2cx2 myocytes are predominant, accounting for at least 50% of the cell population. Multinuclear cells with three to eight diploid nuclei were widespread. The percentage of such cells was five to six times higher in precocial species than in altricial birds of the same weight. Myocytes with polyploid nuclei were rare. A significant interspecies variability of cardiomyocyte ploidy levels was observed. The most prominent differences were found between the precocial and the altricial birds. The mean number of genomes in cells correlated both with the body mass and with the growth rate of the birds. The differences between the precocial and altricial birds disappeared when a statistical method was used to eliminate the effect of the growth rate, but did not when the effect of body mass was eliminated. Among the altricial birds, which are generally immobile during growth, the cardiomyocyte ploidy levels also correlated more closely with growth rate than with body mass. The opposite was observed in the precocial birds, which are highly mobile from the first minutes of life. We conclude that the interspecies variability of bird cardiomyocyte ploidy levels is a result of changes in the balance between the cardiac functional load and the growth rate; this is manifested at the cellular level as a competition between the proliferation and differentiation of cardiomyocytes. J. Exp. Zool. 289:48-58, 2001.     

The manipulation of food resources reveals sex-specific trade-offs between parental self-feeding and offspring care

Parent Palestine sunbirds (Nectarinia osea) feed on flower nectar that is not fed to their nestlings. This phenomenon provided a unique opportunity to manipulate self-feeding rates of parent birds independently of the rate at which they feed arthropod prey to their offspring. Based on provisioning models, we predicted that parents would invest more in their young as the energy content of their own food increased. From our earlier work, we also predicted that the levels of sex-specific activities of males and females would differ as the energy content of their food increased. Sunbird pairs with two or three nestlings were provided with feeders containing a low-, medium- or high-concentration sucrose solution. As the sugar concentration increased, the females delivered arthropods at a greater rate to their nestlings, removed proportionally more faecal sacs and spent longer at the nest, while the males increased their mobbing effort. Nestling food intake and body mass, but not tarsus length or bill size, were larger in small broods than in large broods, and increased with increasing feeder sugar concentration. These results imply that increasing the energy content of food consumed by parent sunbirds allows them to increase the rate at which other foods are delivered to their young and to increase other parental care activities as well. The results also add credence to the idea that behavioural decisions reflect life-history trade-offs between parental self-feeding and investment in current young.     

A poor start in life negatively affects dominance status in adulthood independent of body size in green swordtails Xiphophorus helleri

Whilst there is an abundance of studies revealing how dominance interactions affect access to resources critical for survival and reproductive success, very little is known about how dominance status is influenced by early life experiences. However, there is increasing evidence that early developmental trajectories can shape the physiology and behaviour of the adult. In particular, compensatory growth following a period of poor nutrition can have long-term effects on the phenotype. Since catch-up growth increases daily energy requirements and hence the motivation to acquire sufficient resources, it might either increase or decrease competitive ability and aggression. Here we test whether growth compensation early in life subsequently affects the dominance status of adult male swordtail fishes Xiphophorus helleri, a species with strong sexual dimorphism and male-male competition. Males that experienced a period of restricted food early in life subsequently caught up and achieved the same adult body and ornament size as control males that had been raised on ad libitum food throughout development, but were subordinate to size-matched controls, suggesting a trade-off between sexual attractiveness and competitive ability. This indicates that early life history and/or growth trajectory can be an important determinant of competitive ability independent of current body size.     

Physiological effects of compensatory growth during the larval stage of the ladybird,Cryptolaemus montrouzieri

The growth rate of insects may vary in response to shifty environments. They may achieve compensatory growth after a period of food restriction followed by ad libitum food, which may further affect the reproductive performance and lifespan of the resulting phenotypes. However, little is known about the physiological mechanisms associated with such growth acceleration in insects. The present study examined the metabolic rate, the antioxidant enzyme activity and the gene expression of adult Cryptolaemus montrouzieri (Coleoptera: Coccinellidae) after experiencing compensatory growth during its larval stages. Starved C. montrouzieri individuals achieved a similar developmental time and adult body mass as those supplied with ad libitum food during their entire larval stage, indicating that compensatory growth occurred as a result of the switch in larval food regime. Further, the compensatory growth was found to exert effects on the physiological functions of C. montrouzieri, in terms of its metabolic rates and enzyme activities. The adults undergoing compensatory growth were characterized by a higher metabolic rate, a lower activity of the antioxidant enzymes glutathione reductase, catalase, and superoxide dismutase and a lower gene expression of P450 and trehalase. Taken together, the results indicate that although compensatory growth following food restriction in early larval life prevents developmental delay and body mass loss, the resulting adults may encounter physiological challenges affecting their fitness.     

The effect of a period of food restriction on gonad size and moult of male and female Starlings Sturnus vulgaris under constant photoperiod

The effects of food availability on the reproductive cycle and on the timing and duration of moult were investigated in first-year male and female Starlings Sturnus vulgaris under a constant photoperiod of 12 hours. A 20% lower body mass during the first 9 weeks of restricted feeding had a slight negative effect on testicular growth during the first 3 weeks of the experiment and delayed the onset of moult for 12 days after the return to ad libitum feeding conditions. No effects were found on changes of beak colour and moult duration of males. Females exposed to the shorter feeding time similarly showed a reduced body mass (21%) but compared with controls, did not differ in beak colour, in follicle growth, or in the onset and duration of moult. In contrast to males, body mass of the experimental females after the food restriction period remained lower for more than 6 weeks, compared to control birds. Females had a longer reproductive cycle and started moult later than males. The later an individual started to moult, the faster it moulted. Two females started to moult extremely late and did not moult their first primaries.
These results indicate that in male Starlings food restriction slightly affected the rate of photoinduced gonadal growth and the onset of postnuptial moult. These effects were not observed in females subjected to the same experimental conditions.