The allometric approach to species differences in brain size

Allometric methods can be used to test quantitative theories of the relationship between brain size and body size across species, and to search for ecological, behavioural, life history, and ontogenetic correlates of brain size. Brain size scales with an allometric exponent of around 0.75 against body size across mammals, but is closer to 0.56 for birds and for reptiles. The slope of the allometric line often varies depending upon the taxonomic level of analysis. However, this phenomenon, at least in mammals, may be a statistical artifact. Brain size for a given body size (relative brain size) varies among orders in birds and mammals, and some dietary associations with relative brain size have been found in particular taxa. Developmental status at birth is the most consistent correlate of relative brain size: precocial neonates have larger brains for a given maternal size than altricial neonates in both birds and mammals. Altricial neonates, however, have more brain growth following birth, and in birds also have larger relative adult brain sizes. Energetic explanations for differences in neonatal brain growth, although attractive on theoretical grounds, have largely failed to stand up to empirical tests.     

Embryonic Calls as Care-soliciting Signals in Budgerigars,Melopsittacus undulatus

Embryonic calls occur 1–3 d before hatching among precocial and some altricial birds. In precocial species, calls may synchronize hatching among siblings or, in semi-precocial species, elicit parental attention to, and often thermoregulation of, the hatching egg. Much less is known about the functional significance of calls in fully altricial species. In this study, naturalistic observations and laboratory experiments were used to document factors affecting calling and the parental responses to calls in one altricial species, the budgerigar Melopsittacus undulatus. Budgerigar chicks hatch asynchronously and vocalize 24–48 h before hatching. Embryonic calling rates increase at higher egg temperatures, and also as embryos near hatching. Parents easily locate a calling egg in their clutch, even among a large brood of much older, vocalizing nestlings. Furthermore, they actively assist in the last stages of hatching by helping to break the shell along the crack in the egg. Both observational and experimental evidence suggests that embryonic vocalizations are distinctive signals that increase parental attention and care, and may stimulate hatching assistance to a calling egg.     

Timing of incorporation of docosahexaenoic acid into brain and muscle phospholipids during precocial and altricial modes of avian development

We investigated the possibilities that the proportion of docosahexaenoic acid (DHA) in phospholipids of brain and skeletal muscle at hatch, and the ontogenetic timing of the DHA accretion spurt in these tissues, might serve as indices of neonatal functional maturity that discriminate between precocial and altricial avian developmental modes. Comparison of the fatty acid profiles of the initial and residual yolks of two free-living altricial species, the swallow (Hirundo rustica) and the sparrow (Passer domesticus), reveals that, in contrast to precocial birds, there is no preferential uptake of DHA from the yolk during embryonic development. At hatch, the proportions of DHA in brain phospholipid (wt.% of fatty acids) of the swallow and sparrow, at 8.1% and 5.0%, respectively, are far lower than the values (16.9-19.6%) reported for non-altricial species. This reflects a marked difference in the timing of the brain DHA accretion spurt, which occurs during the first half of the embryonic period of precocial birds, but is largely delayed until after hatching in the altricial species. By the time of fledging, the proportion of DHA in the swallow brain phospholipid has increased to 14.3%. For non-altricial birds, the brain DHA concentration at hatch shows little interspecies variation, despite major differences in yolk DHA content. The proportions of DHA in leg muscle phospholipid of the newly hatched swallow and sparrow, at 2.9% and 2.5%, respectively, are far lower than the value (6.7%) for the precocial chicken. Again, this relates to differences in developmental timing, with muscle DHA accretion occurring in the first half of the chicken's embryonic period, whereas, in the swallow, this increase is delayed until after hatching. By the time of fledging in the swallow, DHA forms 9.3% of muscle phospholipid fatty acids, equivalent to the level attained in chicken muscle at the mid-embryo stage. The results indicate a clear distinction between altricial and non-altricial avian species in the timing of tissue DHA accretion during development, presumably reflecting differences in neonatal functional maturity.     

The Expensive Brain: A framework for explaining evolutionary changes in brain size

To explain variation in relative brain size among homoiothermic vertebrates, we propose the Expensive Brain hypothesis as a unifying explanatory framework. It claims that the costs of a relatively large brain must be met by any combination of increased total energy turnover or reduced energy allocation to another expensive function such as digestion, locomotion, or production (growth and reproduction). Focusing on the energetic costs of brain enlargement, a comparative analysis of the largest mammalian sample assembled to date shows that an increase in brain size leads to larger neonates among all mammals and a longer period of immaturity among monotokous precocial species, but not among the polytokous altricial ones, who instead reduce their litter size. Relatively large brained mammals, altricial and precocial, also show reduced annual fertility rates as compared to their smaller brained relatives, but allomaternal energy inputs allow some cooperatively breeding altricial carnivores to produce even more offspring in a shorter time despite having a relatively large brain. Thus, the Expensive Brain framework explains why brain size is linked to life history pace in some, but not all mammalian lineages. This framework encompasses other hypotheses of energetic constraints on brain size variation and is also compatible with the Brain Malnutrition Risk hypothesis, but the absence of a mammal-wide correlation between brain size and immature period argues against the Needing-to-Learn explanation for slower development among large brained mammals.     

Comparative growth rates and oxygen consumption in young Galliformes

The high correlation between growth rate and adult body weight has been much more thoroughly documented for altricial birds than for precocial species. This paper gathers data from the literature for precocial Galliformes and also reports new growth data on six galliform species for analysis. The onset of homeothermic ability is investigated in Galliformes over a range of body size. The results confirm that (1) large species' chicks grow at a slower rate than those of smaller species, and (2) larger species' chicks can thermoregulate earlier than smaller species' chicks under cold stress situations. Published embryonic body weights are also analysed to determine when growth rate differences appear in the development of precocial species. No interspecific differences appeared in the relative growth rates of embryos, and therefore species body size does not appear to influence growth rate before hatching.     

Ontogenetic development of the ophthalmic rete in relation to brain cooling in chickens and pigeons

The brain cooling capacity of the altricial pigeon increases during posthatching growth at a higher rate than that of the precocial duck and chicken. To determine if this difference between the altricial and the precocial modes of development can be related to growth rates of the vascular heat exchanger involved in brain cooling (the ophthalmic rete), we performed a morphometric analysis of this structure during the post-hatching maturation of the three species. The number of vascular units in the rete did not change during development but differed significantly among species. The retia continued to grow in length and diameter in an exponential relation with body mass at similar rates in all species. The surface area of the retial arteries, which reflects the area available for countercurrent heat exchange, also increased exponentially with body mass, but without significant differences among the three species. However, the effectiveness of the rete in brain cooling, as indicated by the degree of brain cooling per unit of heat-exchange area in the rete, was higher in the altricial pigeon than in the precocial chicken and duck. It is concluded that the posthatching morphometric changes in the ophthalmic rete (rete ophthalmicum) are important for the development of brain cooling capacity, but cannot solely explain differences in brain cooling between growing altricial and precocial birds. These differences are most likely related to differences in the maturation of the central thermoregulatory control system and the peripheral effector mechanisms among the two groups of birds.     

Eggshell structure, mode of development and growth rate in birds

The shell of an egg contributes to successful embryogenesis in many ways, such as through protection, respiration and water exchange. The shell is also the major source of calcium for the development of high-calcium consuming organs, e.g. the skeleton, muscles and brain. Some studies show, moreover, that growth rate may play a fundamental role in the pattern of skeletal development in birds: the faster the growth the less ossified the skeleton is at hatching. We predicted, therefore, that slow (precocial) and fast (altricial) growing bird species should lay eggs encased in shells with different structures adapted to support different rates of calcium removal by developing embryos. We tested this prediction by comparing the fine structure of the inner eggshell surface (mammillary layer) from 36 bird species belonging to 18 orders ranging from Struthioniformes to Passeriformes. Using scanning electron microscopy, we compared the mammillary layer of both non-incubated eggs and eggs at the time of hatching, i.e., before and after embryonic development and the accompanying calcium removal. The results were consistent with the prediction, i.e., the number of mammillary tips per unit of surface area was associated with mode of development and growth rate. The number was higher, and calcium removal was also more extensive, in shells from precocial bird species than in shells from altricial bird species.     

HOW MAMMALS PRODUCE LARGE-BRAINED OFFSPRING

Two explanations for species differences in neonatal brain size in eutherian mammals relate the size of the brain at birth to maternal metabolic rate. Martin (1981, 1983) argued that maternal basal metabolic rate puts an upper bound on the mother's ability to supply energy to the fetus, thereby limiting neonatal brain size. Hofman (1983) proposed that gestation length in mammals is constrained by maternal metabolic rate, implying an indirect constraint on neonatal brain size. Since individuals of precocial species have much larger neonatal brain sizes and are gestated longer for a given maternal body size than individuals of altricial species, Martin's and Hofman's ideas also require that mothers of precocial offspring have higher metabolic rates for their body sizes than mothers of altricial offspring. Data on 116 mammal species from 13 orders show that neither neonatal brain size nor gestation length is correlated with maternal metabolic rate when maternal body-size effects are removed. For a given maternal size, there is no difference in metabolic rates between precocial and altricial species, despite a two-fold difference between them in average neonatal brain size. However, neonatal brain size is strongly correlated with gestation length and litter size, independently of maternal size and metabolic rate. Analyses conducted within orders replicated the findings for gestation length and suggested that neonatal brain size may be at best only weakly related to metabolic rate. Differences in neonatal brain size appear to have evolved primarily with species differences in gestation length and litter size but not with differences in metabolic rate; large-brained offspring are typically produced from litters of one that have been gestated for a long time relative to maternal size. We conclude that species differences in relative neonatal brain size reflect different life-history tactics rather than constraints imposed by metabolic rate.     

Changes in catecholamines and dopaminergic metabolites in pigeon brain during development from the late embryonic stage toward hatch

While brain development during embryogenesis has been extensively studied in precocial birds, there is no information available on altricial birds. Thus, the concentrations of the catecholamines norepinephrine (NE), epinephrine (E), and dopamine (DA), and the dopaminergic metabolites 3,4-dihydroxyphenylacetic acid (DOPAC) and 4-hydroxy-3-methoxyphenylacetic acid (HVA) were determined at several stages during the late embryonic period (E13, E14, E15, E16, E17 and E18) and the day-of-hatch (P0) in the pigeon telencephalon, cerebellum, optic lobe, and brainstem. The concentrations of all catecholamines were higher than those reported in chicken embryos. During embryogenesis, NE, E, DOPAC and HVA concentrations in the various brain parts increased throughout embryonic development until shortly before hatching at which time they decreased. DA, however, continued to increase through hatching in the brainstem, and the changes in DA concentrations varied in several brain parts. In conclusion, catecholamine concentrations in the various brain parts tended to increase with embryonic age, and the concentrations were higher than those in chickens. Furthermore, brain catcholamine metabolism changed at hatch in pigeons.     

晚成性哺乳动物体温调节能力的胎后发育

按照体温调节能力的发育情况,哺乳动物的生长发育可分为早成性、晚成性和未成熟性3类。本文主要综述了晚成性哺乳动物体温调节能力的发育特点。这类动物的幼体出生时一般身体裸露,热传导率较高,产热能力较差,不能进行有效的体温调节。当环境温度低于热中性区时,单独的个体不能维持较高的恒定体温。但晚成性幼体也具有一定的体温调节能力,当受低温刺激时,即使新生幼体也会具有增加代谢率的反应;同时结合亲体关怀和幼体之间的聚群效应以及巢的保温作用等方式,仍能使其体温维持在一个较高的水平。晚成性幼体生理性产热的不足,也可看作是一种有利的特点,这样可以减少能量在体温调节方面的消耗,从而增加用于生长发育的能量。文章最后对可能的发展方向进行了展望。     

Active and resting metabolism in birds: allometry, phylogeny and ecology

Variation in resting metabolic rate is strongly correlated with differences in body weight among birds. The lowest taxonomic level at which most of the variance in resting metabolic rate and body weight is evident for the sample is among families within orders. The allometric exponent across family points is 0.67. This exponent accords with the surface area interpretation of metabolic scaling based on considerations of heat loss. Deviations of family points from this allometric line are used to examine how resting metabolic rates differ among taxa, and whether variation in resting metabolic rate is correlated with broad differences in ecology and behaviour. Despite the strong correlation between resting metabolic rate and body weight, there is evidence for adaptive departures from the allometric line, and possible selective forces are discussed.
The allometric scaling of active metabolic rate is compared with that of resting metabolic rate. The allometric exponents for the two levels of energy expenditure differ, demonstrating that active small-bodied birds require proportionately more energy per unit time above resting levels than do active large-bodied birds. No consistent evidence was found to indicate that the different methods used to estimate active metabolic rate result in systematic bias. Birds require more energy relative to body size when undertaking breeding activities than at other stages of the annual cycle.     

A comparative study of embryonic development of some bird species with different patterns of postnatal growth

Some studies show that birds with high postnatal growth rates (e.g. altricial species) are characterized by a rapid early development of "supply" organs, such as digestive organs. Birds with low postnatal growth rates (e.g. precocial species) exhibit a slower early development of these organs and a more rapid early development of other "demand" organs, such as brain, muscles, skeleton and feathers. To test whether these differences can be traced back to early embryonic development and whether they can be associated with changes in developmental timing, i.e. heterochrony, we compared embryos of the precocial quail and the altricial fieldfare, two bird species with low and high postnatal growth rates, respectively. We used classical staging techniques that use developmental landmarks to categorize embryonic maturity as well as morphological measurements. These techniques were combined with immune detection of muscle specific proteins in the somites. Our data showed that the anlagen of the head, brain and eyes develop earlier in the quail than in the fieldfare in contrast to the gut which develops earlier in the fieldfare than in the quail. Our data also showed that the quail and the fieldfare displayed different rates of myotome formation in the somites which contribute to muscle formation in the limbs and thorax. We believe these observations are connected with important differences in neonatal characteristics, such as the size of the brain, eyes, organs for locomotion and digestion. This leads us to the conclusion that selection for late ontogenetic characteristics can alter early embryonic development and that growth rate is of fundamental importance for the patterning of avian embryonic development. It also appears that this comparative system offers excellent opportunities to test hypotheses about heterochrony.     

FISHER'S SEX RATIO THEORY MAY EXPLAIN HATCHING PATTERNS IN BIRDS

I present the hypothesis that asynchronous hatching is a means of ensuring an equal degree of parental investment in the progeny of each sex in altricial species of birds that are sexually dimorphic in size. In a comparative analysis of bird species of Africa and the Western Palearctic, I find a positive relationship between hatching asynchrony and sexual size dimorphism, in support of the hypothesis. The relation is significant for species in which males are larger than females, and in species in which females are larger than males. In addition, it holds even if allometric effects of body size are controlled for. No such relationship is found in species with self-feeding young. Alternative hypotheses to explain asynchronous hatching in altricial birds are discussed. The results of the comparative study are also consistent with some of these hypotheses. For instance, asynchronous hatching may be a mechanism used by parents of dimorphic species to deal with unpredictable primary sex ratios; it may be a way of avoiding simultaneous peak food demands by the young; or it may be a way of advancing the time of hatching so that the division of labor between the parents is optimized.     

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 separate effects of egg size and parental quality on the development of ornamental plumage coloration

The fitness‐related consequences of egg size, independent of the influences of parental quality, are poorly understood in altricial birds. Not only can egg size and parental quality influence growth and survival, but each could influence the development of condition‐dependent plumage coloration in offspring. The Eastern Bluebird Sialia sialis is an altricial, multi‐brooded, cavity‐nesting passerine in which juveniles display dichromatic UV‐blue plumage. Previous research suggests that plumage coloration acts as a signal of individual quality among juvenile and adult Eastern Bluebirds. Here, we separate the effects of egg size and parental quality (defined by egg size laid) on nestling growth and plumage ornamentation by exchanging clutches of large eggs with clutches of small eggs. Nestlings were significantly larger immediately post‐hatching when hatched from a large egg, but to maintain a larger size, nestlings needed to have hatched from a large egg and to have been reared by high‐quality parents. Nestlings were brighter when reared by high‐quality parents and this relationship was strongest later in the breeding season. Nestlings exhibited greater UV chroma if hatched early in the season, but UV chroma was not significantly affected by egg size or parental quality. These findings demonstrate varying influences of both egg size and parental quality on offspring growth and plumage ornamentation but suggest that quality of post‐hatching investment is more influential than pre‐hatching investment.     

Mode of development and interspecific avian brood parasitism

Avian interspecific brood parasites differ considerably in theircommitment to parasitism; 87 species are obligate brood parasites,whereas 35 species are known to be facultative brood parasites.This variation is strongly related to mode of development. Obligateparasitism is found almost exclusively in altricial species,whereas facultative interspecific parasitism is predominantin precocial birds. We propose that the association betweenmode of development and form of parasitism reflects a fundamentaldifference between altricial and precocial birds in the relativebenefits of emancipation from parental care after laying. Weargue that altricial brood parasites obtain such a large increasein realized fecundity by avoiding the costs of parental carethat obligate parasitism is favored over facultative parasitism.In contrast, precocial brood parasites gain relatively littlein terms of increased fecundity via obligate parasitism, andmuch of this increase could potentially be gained by facultativeparasitism. Thus, obligate interspecific brood parasitism willnot be favored in precocial birds. Three factors influence thisdifference between altricial and precocial species: (1) altricialbirds have relatively more energy and nutrients with which tolay additional eggs, (2) altricial birds can produce more eggsfor the same amount of energy and nutrients, and (3) altricialbirds realize a greater relative gain in fecundity for eachadditional egg laid. We suggest further that facultative interspecificparasitism in birds may originate simply through a carry overof intraspecific parasitism; 29 of 33 facultative interspecificparasites also parasitize conspecifics. Facultative parasitismof other species would provide a greater range of potentialhost nests and could be maintained as an evolutionarily stableend point by the same mechanisms that maintain intraspecificbrood parasitism. [Behav Ecol 1991;2:309–318]     

Altricial and precocial mammals: A model of neural and muscular development

This model of growth offers a quantitative definition for altricial and precocial newborns, makes muscular strength a benchmark for locomotor independence, and discriminates related genera as well as genera across major taxonomic divides. The model contrasts four theoretical conditions of the neonate (I, small brain, weak musculature; II, small brain, strong musculature; III, large brain, weak musculature; IV, large brain, strong musculature) with species from three orders of placental mammal. Each species exhibits a distinct mother-infant strategy from the altricial red panda cub (condition I) and the golden lion tamarin (condition III) to the precocial wildebeest calf (condition IV). The model proposes that early growth rates of brain and muscle correlate with nutrition, maternal effort during gestation and lactation, and parental care, whereas postnatal muscular growth correlates directly with adult body size and locomotor repertoire. An example of condition II (small brain, strong musculature) has not been found. This suggests that muscle does not grow in advance of the brain and that the brain acts as a pacemaker of growth. In order to increase our understanding of exotic species, noninvasive measures (body weight and length) and observations (opening of the eyes and ears, hair density, weaning, and the abilities to ther-moregulate and to move) should be supplemented with analysis of the differential tissue and organ growth. In both theoretical and practical ways analysis of deceased individuals contributes to the understanding of all species.     

Development of cardiac rhythms in birds

Heart rate (HR) in avian embryos developing inside an eggshell has been measured by various means while maintaining adequate gas exchange through the eggshell. This is an important requirement in order to avoid adverse effects of impeding gas exchange on the cardiac rhythms of developing embryos. The present report is a review of our ontogenetic study on embryonic HR, which was measured with fulfillment of the above requirement and also hatchling HR measured non-invasively. Firstly, we reviewed measurements of daily changes (developmental patterns) in embryonic mean heart rate (MHR), which were determined from a short-term measurement of HR once a day, in 34 species of altricial and precocial birds. The allometric relationship between the MHR during pipping in altricial birds and their fresh egg masses was the same as that between the MHR at 80% of incubation duration and fresh egg masses in pre-cocial birds. Secondly, we presented the developmental patterns of MHR in chick embryos and hatchlings, which were determined from long-term, continuous measurement of HR before, during and after hatching. The ultradian and circadian rhythms of HR were clearly shown in embryos and hatchlings, respectively. Thirdly, we summarized instantaneous HR fluctuations: HR variability and HR irregularities, in chick embryos and hatchlings. The distinctive patterns were shown in pre-pipped and pipped embryos and newly hatched chicks, individually, which were partly related to autonomic nervous functions and physiological functions.     

Catch-up growth in Japanese quail (Coturnix Japonica): relationships with food intake, metabolic rate and sex

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 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.     

Post-hatching parental care behaviour and hormonal status in a precocial bird

In birds, the link between parental care behaviour and prolactin release during incubation persists after hatching in altricial birds, but has never been precisely studied during the whole rearing period in precocial species, such as ducks. The present study aims to understand how changes in parental care after hatching are related to circulating prolactin levels in mallard hens rearing ducklings. Blood was sampled in hens over at least 13 post-hatching weeks and the behaviour of the hens and the ducklings was recorded daily until fledging. Contacts between hens and the ducklings, leadership of the ducklings and gathering of them steadily decreased over post-hatching time. Conversely, resting, preening and agonistic behaviour of hens towards ducklings increased. Plasma prolactin concentrations remained at high levels after hatching and then fell after week 6 when body mass and structural size of the young were close to those of the hen. Parental care behaviour declined linearly with brood age, showed a disruption of the hen-brood bond at week 6 post-hatching and was related to prolactin concentration according to a sigmoid function. Our results suggest that a definite threshold in circulating prolactin is necessary to promote and/or to maintain post-hatching parental care in ducks.