2.1.1. Maturity of hatchlings

The development of homeothermy is closely related to the maturational state of a hatchling. Newly-hatched chicks of different species of birds vary markedly in the maturity of many anatomical, physiological and behavioural aspects. In regard to hatchling maturity and the pattern of post-hatching development, birds are divided into two main groups: precocial and altricial. In addition, the terms “semiprecocial” and “semialtricial” are commonly used to name intermediate forms of the two main groups. Different further subdivisions are made by Nice (1962), Skutch (1976) and Starck (1993). The latter, for example, divides altricials and precocials into two and three subgroups, respectively, and names the most developed precocials as superprecocials (family Megapodidae). The precocial–altricial classification has also been adapted for mammals.

At hatching, precocial chicks have downy coats and well-developed nervous and muscular functions (e.g. Starck 1993). The chicks leave the nest soon after hatching, and they are frequently exposed to ambient temperatures below the thermoneutral zone. This is enabled by an ability to increase heat production soon after hatching (Matthew 1983). Semiprecocials also have downy plumage and open eyes, and they are able to walk outside the nest shortly after hatching. However, they differ from precocials in that they stay within the nest or nesting area for a longer time while food is brought to them by their parents (Starck 1993). The thermoregulatory ability of semiprecocials is comparable to that of precocials.

Altricial nestlings hatch totally or almost without plumage and eyes closed, and they exhibit little motor activity other than begging (Ricklefs 1973, Starck & Ricklefs 1998a). Altricials are totally unable to survive without parental feeding and heating. The body temperature of altricials corresponds passively to changes in ambient temperature, indicating that altricials are poikilothermic and lack thermoregulatory heat production. Semialtricials have somewhat better insulative down, may hatch with their eyes open and show more movement activity.

Precociality and altriciality represent two different strategies for the allocation of energy to the reproduction. On the one hand, precocial eggs and chicks require large energy commitments from parents, the post-hatching energy investments going mainly into protection activity (Dunn 1980). Altricial species, on the other hand, require extensive energy input from the parents in the form of feeding and heating. Due to these different strategies, the stage of development at hatching, the post-hatching maturation speed, and the ability to move and thermoregulate, all vary considerably between the chicks of the two main patterns.

More quantitative bases for the classification of hatchling maturity have also been used. Carey et al. (1980) classified hatchlings based on the yolk content of the newly laid egg, a positive correlation being found between the hatchling maturity and the proportion of yolk in the egg. Yolk content is related to hatchling maturity because the development of the most mature forms requires a larger amount of energy in the form of yolk (Whittow & Tazawa 1991). Ricklefs (1983) and Starck and Ricklefs (1998a) presented the use of water content or the inversely dry matter content of a tissue as an index of the tissues functional maturity and more comprehensively as a way of describing the state of maturation of hatchlings. Lean dry matter content increases with age in nearly all tissues and species. Furthermore, it is usually well correlated with other functional measures such as enzyme activities in skeletal muscles, and it is also inversely correlated with growth rate.

2.1.2. Post-hatching development

Most juvenile birds have only a limited capability to maintain their body temperature in a cold environment. Small body size and weak insulation expose chicks to heat loss. Because of their limited ability to increase heat production, chicks tolerate ambient temperatures only slightly lower than the lower critical temperature (LCT). The post-hatching development of thermoregulation appears in the ability to sustain constant body temperature at gradually decreasing ambient temperatures and for a longer time period. The ability to both produce extra heat and to prevent heat loss during a cold spell are the basic factors of thermoregulation (for a review, see Visser 1998). In newly-hatched birds, the thermoneutral zone (TNZ) is narrow and in practice there may be just one thermo-neutral temperature rather than a zone (e.g. Mathiu et al. 1991). During post-hatching development, the zone gets broader due to the development of insulative plumage and increased metabolism. The lower critical temperature, which determines the lower end of the thermoneutral zone, can be estimated from the equation

Equation 1.

where K is the minimum thermal conductance and RMR is the resting metabolic rate. Consequently, high RMR and low K results in low LCT. To maintain body temperature unchanged in ambient temperatures lower than the LCT, the metabolic rate (MR) must be increased by means of regulatory thermogenesis equalling heat loss:

Equation 2.

The magnitude of peak metabolic rate (PMR) and the time-period that it can be sustained for are important factors in regulatory thermogenesis. Although the opportunities for heat production and prevention of heat loss are limited, juvenile birds can partly compensate for these limitations by behavioural thermoregulation and the good endurance of hypo-thermia. Chicks also benefit from their low body temperature, which is lower than that of adult birds. The low body temperature entails smaller thermal gradient and consequently smaller heat loss to the surroundings.

Even though the embryos of some precocial species are capable of slightly increasing heat production in response to acute cold exposure (e.g. Steen & Gabrielsen 1988, Whittow & Tazawa 1991), the escape from the egg shell in hatching is the major step enabling increased ventilation, heat production by aerobic metabolism and thermo-regulation (Mathiu et al. 1991). During internal and external pipping, the mechanism used for gas exchange passes from the chorioallantoic membrane to the lungs. Internal pipping occurs when the embryo accesses the egg air cell by piercing the chorioallantoic membrane and the inner shell membrane with its beak. In external pipping, the embryo breaks the eggshell with its egg tooth.

In precocial chicks, the capability for significant regulatory thermogenesis usually appears within a few hours of hatching, after the hatching down has dried. The prerequisite for the regulatory thermogenesis is the maturity of the skeletal muscles and the neuronal control of these muscles. In altricial birds, the required maturation level is achieved only during post-hatching development and therefore regulatory thermogenesis is not possible until several days after hatching. Precocial chicks benefit from the early attainment of homeothermy since it permits independent food seeking for longer foraging periods, thus enabling increased energy intake. However, this early homeothermy generally incurs higher metabolic costs for the chicks and thus limits their growth rate. The growth rate of precocial birds is 3–4 times slower than in altricial chicks of the same asymptotic body mass (Ricklefs 1979). High functional maturity seems to be in-compatible with high growth rate. In altricial nestlings, energy is allocated mainly to growth at the cost of the maturity needed for thermoregulation.

In most precocial and semiprecocial birds, the mass-specific resting metabolic rate in thermoneutrality shows a swift increase during the first post-hatching days or week (Koskimies 1962, Freeman 1967, Palokangas & Hissa 1971, Bernstein 1973, Blem 1978, Hissa et al. 1983, Matthew 1983, Spiers et al. 1985, Klaassen & Bech 1992, Sutter & MacArthur 1992, Visser & Ricklefs 1993, Dietz et al. 1995). After the maximum is reached, the mass-specific resting metabolic rate decreases, finally approaching the level existing in adult birds. At the inflexion point, chick mass is approximately 25% of adult mass (Weathers & Siegel 1995). The physiological basis for the biphasic pattern is somewhat unclear. The increasing phase of the pattern is probably linked to an increase in the oxidative capacity of organs, an increase in the relative proportion of metabolic active tissues, the increasing mass and function of gut and heart, and the absorption of metabolically inactive residual yolk (Dietz et al. 1995). The subsequent decreasing phase may be related to a decrease in the proportion of metabolically active tissue, due for example to the deposition of fat (Weathers & Siegel 1995). However, since the oxidative capacity of muscle tissue increases continuously during development (Choi et al. 1993, Dietz & Ricklefs 1995, Dietz & Ricklefs 1997), the heat production capacity of metabolically active tissue probably does not decrease after the inflexion point (Dietz et al. 1995). In altricial nestlings, the mass-specific resting metabolic rate usually increases linearly to the adult level (Weathers & Siegel 1995, Visser 1998). There is some evidence, however, that suggests that a biphasic pattern can also exist in large-sized altricials, e.g. in white-necked ravens, Corvus cryptoleucus (Mishaga & Whitford 1983).

The heat produced by the resting metabolism can only be used to a minor extent in sustaining a constant body temperature in ambient temperatures below LCT. The peak metabolic rate is more essential for this purpose. In newly-hatched altricials, the PMR equals the resting metabolic rate, indicating both the lack of regulatory thermogenesis and the fact that nestlings are poikilothermic (Weathers & Siegel 1995). Furthermore, cold exposure strongly reduces heat production when body temperature decreases. At some point in post-hatching development, nestlings attain the ability to increase heat production in response to cold exposure. For example, in bank swallows (Riparia riparia), this ability appears suddenly at the age of 8 days (Marsh & Wickler 1982) and in European starlings, Sturnus vulgaris, at 6 days of age (Ricklefs & Webb 1985). Newly-hatched precocial chicks, when exposed to moderate cold of 20°C, are able to increase their heat production 1.4-5 times above the resting metabolic rate (Visser 1998). During subsequent development, the increase in the PMR results from maturation and increase of body mass. In particular, the increase of muscle mass and the muscle-mass-specific heat production are important determinants.

Two major muscle groups can be found in birds, namely leg and flight muscles. Flight or breast muscles (m. pectoralis and m. supracoracoideus) constitute the largest and most energy-consuming tissues in adult volant birds (Marsh & Dawson 1989, Butler 1991). For most newly-hatched precocials and semiprecocials, the leg muscles are the principal site of regulative thermogenesis because of their larger mass and higher level of maturity in comparison to the breast muscles. For example, young galliforms seem to rely primarily on leg muscles in thermogenesis although they can fly at a relatively early age (Choi et al. 1993). Aulie and Grav (1979) calculated that even in 2-week-old bantam chicks, the total respiratory capacity of the leg muscles is 3.4 times higher than that of the pectorals. However, some exceptions may occur among precocials. In Procellariiformes, chicks have relatively large breast muscles whose dry matter content is similar to that of their leg muscles (Visser 1998). This finding possibly indicates that breast muscles also have a significant role in thermogenesis. During precocial post-hatching development, the breast muscles gradually grow larger in mass and assume the principal task in heat production. In newly-hatched capercaillie (Tetrao urogallus), the pectoral muscles comprise only 2.5% of the total heat production, but at the age of 80–105 d the pectorals already produce 21% of the total heat (Saarela et al. 1990). In altricial species, the breast muscles are important heat producing tissues when thermogenesis in cold appears, even though their mass may be smaller than (Morton & Carey 1971, Olson 1994) or equal to the mass of the leg muscles (Marsh & Wickler 1982, Ricklefs & Webb 1985).

At hatching, thermal conductance is dependent on the insulative structures and the size of the chick. In precocial chicks, minimum thermal conductance either decreases steadily during post-hatching development (Hissa et al. 1983, Spiers et al. 1985, Sutter & MacArthur 1992, Gdowska et al. 1993) or most rapidly within the first post-hatching week (Eppley 1984, Ricklefs et al. 1984). The two latter studies showed that a significant decrease in conductance may occur without apparent plumage growth. The change is obviously due to an increase in the effectiviness of the vasomotor control of peripheral circulation. In altricial nestlings, the thermal insulation of the nest and huddling enable effective homeothermy for the whole brood even before the completion of plumage growth and before the individual nestling is homeothermic outside of the nest (e.g. Diehl & Myrcha 1973, Clark 1982, Mayer et al. 1982).

The development of temperature regulation can be described using the index of homeothermy, I_h, which represents the ability to maintain body temperature during cold exposure in relation to initial or adult body temperature:

Equation 3.

Theoretically, in totally poikilothermic chicks, the value of the index is 0 and in adult birds 1. The prerequisite for the use of the index is the standardization of both temperature and duration of cold exposure (Ricklefs 1987). In altricial species, the homeothermic index shows a three-phasic development that can be illustrated with a steep sigmoid curve (Shichun et al. 1979, Weathers 1996). In the first phase, the index remains unchanged. In the second, a rapid increase occurs, and in the third phase, the index levels off after a slight increase. These phases correspond to the three stages that Morton & Carey (1971) have observed in the homeothermic development of nestling Passeriformes. The first stage is a period of maximal growth when the nestling is totally dependent on parents as the heat source. The second stage is a rapid transition phase, and the third is a period of thermal independence when feather growth continues and mass increase ceases. In precocial turkeys (Meleagris gallopavo), guinea fowls (Numida meleagris) (Dietz & van Kampen 1994) and Muscovy ducklings (Cairina moschata) (Harun et al. 1997), the homeothermic index shows a quantum leap during first two post-hatching days and thereafter only a small increase occurs. In newly-hatched precocial shorebirds, the index increases with body size, partly reflecting increased thermal inertia with increasing body mass (Visser & Ricklefs 1993).