Mechanisms promoting higher growth rate in arctic than in temperate shorebirds

Abstract

We compared prefledging growth, energy expenditure, and time budgets in the arctic-breeding red knot (Calidris canutus) to those in temperate shorebirds, to investigate how arctic chicks achieve a high growth rate despite energetic difficulties associated with precocial development in a cold climate. Growth rate of knot chicks was very high compared to other, mainly temperate, shorebirds of their size, but strongly correlated with weather-induced and seasonal variation in availability of invertebrate prey. Red knot chicks sought less parental brooding and foraged more at the same mass and temperature than chicks of three temperate shorebird species studied in The Netherlands. Fast growth and high muscular activity in the cold tundra environment led to high energy expenditure, as measured using doubly labelled water: total metabolised energy over the 18-day prefledging period was 89% above an allometric prediction, and among the highest values reported for birds. A comparative simulation model based on our observations and data for temperate shorebird chicks showed that several factors combine to enable red knots to meet these high energy requirements: (1) the greater cold-hardiness of red knot chicks increases time available for foraging; (2) their fast growth further shortens the period in which chicks depend on brooding; and (3) the 24-h daylight increases potential foraging time, though knots apparently did not make full use of this. These mechanisms buffer the loss of foraging time due to increased need for brooding at arctic temperatures, but not enough to satisfy the high energy requirements without invoking (4) a higher foraging intake rate as an explanation. Since surface-active arthropods were not more abundant in our arctic study site than in a temperate grassland, this may be due to easier detection or capture of prey in the tundra. The model also suggested that the cold-hardiness of red knot chicks is critical in allowing them sufficient feeding time during the first week of life. Chicks hatched just after the peak of prey abundance in mid-July, but their food requirements were maximal at older ages, when arthropods were already declining. Snow cover early in the season prevented a better temporal match between chick energy requirements and food availability, and this may enforce selection for rapid growth.

Appendix

Simulation model

The simulation model predicts body mass, foraging time, energy requirements and required metabolisable energy intake of red knot and common redshank chicks during an 18-day fledging period, on the basis of growth, time budget and metabolism data reported in this paper or from the literature. We distinguished two environments differing in daylength (D, h/day) and operative temperature (T _e, °C): arctic (D=24 h/day, T _e=3°C, data from Cape Sterlegov) and temperate (D=16 h/day, T _e=15°C, data from The Netherlands, May–June 1992–1995).

At each age t, body mass (M, g) of chicks was predicted from a logistic growth curve:

• knot:

$$ M{\rm{ = 120 / [1 + 8}}{\rm{.23 e}}^{{\rm{ - 0}}{\rm{.240 }}t} {\rm{] (this}}\;{\rm{study)}} $$

(1)

• redshank:

$$ M{\rm{ = 109 / [1 + 6}}{\rm{.17 e}}^{{\rm{ - 0}}{\rm{.137 }}t} {\rm{] (from}}\;{\rm{Beintema}}\;{\rm{and}}\;{\rm{Visser}}\;{\rm{1989b)}} $$

(2)

The proportion of daylight time that chicks were brooded by a parent (B) was calculated by inserting mass and T _e into logistic regression equations derived from our time budget observations (Tables  1, 2). As too few observations with rain were made for knots to estimate its effect on brooding time, we used the equations for dry weather in both species:

• knot:

$$ {\rm{logit(}}B{\rm{) = 5}}{\rm{.22 - 0}}{\rm{.160 }}M{\rm{ + 0}}{\rm{.027 }}T_{\rm{e}} $$

(3)

• redshank:

$$ {\rm{logit(}}B{\rm{) = 8}}{\rm{.02 - 0}}{\rm{.160 }}M{\rm{ + 0}}{\rm{.401 }}T_{\rm{e}} $$

(4)

Potential foraging time (FT, h/day) was calculated as day length minus brooding time. Redshank chicks do not forage during darkness (personal observation). We made calculations including and excluding the condition that chicks need 6 h of sleep each day, to show the effect of this requirement. We assumed that temperate chicks fit this into the 8-h night, while arctic chicks sleep whenever brooded and reduce foraging time only if daily brooding time is less than time required for sleep (i.e., if B<0.25):

• arctic:

$$ {\rm{FT = 24 - (24 }}B{\rm{)}}\;\;{\rm{if }}B{\rm{ }} \ge {\rm{ 0}}{\rm{.25 ;}}\;\;F{\rm{ = }}D{\rm{ }}S\;\;{\rm{if }}B{\rm{ < 0}}{\rm{.25}} $$

(5)

• temperate:

$$ {\rm{FT = 16 - (16 }}B{\rm{)}} $$

(6)

In a balanced budget, total metabolisable energy intake over the hours spent foraging equals energy metabolised over the entire 24-h period (ME, kJ/day). Hence, required metabolisable energy intake rate while foraging (RI, J/s) at each age was calculated as:

$$ {\rm RI = ME / (3}{\rm .6 FT)} $$

(7)

ME is the sum of daily energy expenditure as measured with DLW (DEE, kJ/day) and energy incorporated into tissue (E _tis, kJ/day):

$$ {\rm{ME = DEE + }}E_{{\rm{tis}}} \;\;{\rm{if}}\;{\rm{ }}E_{{\rm{tis}}} {\rm{ > 0 ;}}\;\;\;{\rm{ME = DEE}}\;\;{\rm{if}}\;{\rm{ }}E_{{\rm{tis}}} \le {\rm{0}} $$

(8)

E _tis was calculated as the daily increment of the product of body mass and energy density, the latter estimated from the fraction of adult mass attained (see Materials and methods):

• knot:

$$ E_{{\rm{tis}}} {\rm{ = }}M_{t{\rm{ + 1}}} \left[ {{\rm{4}}{\rm{.38 + 3}}{\rm{.21 }}M_{t{\rm{ + 1}}} {\rm{/120}}} \right]{\rm{ - }}M_t \left[ {{\rm{4}}{\rm{.38 + 3}}{\rm{.21}}M_t {\rm{/120}}} \right] $$

(9)

• redshank:

$$ E_{{\rm{tis}}} {\rm{ = }}M_{t + 1} {\rm{ }}\left[ {{\rm{4}}{\rm{.38 + 3}}{\rm{.21}}\,M_{t{\rm{ + 1}}} {\rm{ / 109}}} \right]{\rm{ - }}M_t {\rm{ }}\left[ {{\rm{4}}{\rm{.38 + 3}}{\rm{.21 }}M_t {\rm{ / 109}}} \right] $$

(10)

For DEE of knot chicks, we used the equation derived in Results, inserting T _e=3°C. Because DEE was not measured in common redshank, we used the mass-DEE relationship for black-tailed godwit chicks (Schekkerman and Visser 2001). This relation did not differ significantly from that for northern lapwings, despite considerable differences in age at the same mass, hence we assumed that it applies to redshank as well. The equation is based on DLW measurements made at a mean T _e of 15°C.

• knot:

$$ {\rm{DEE = 2}}{\rm{.630 }}M^{{\rm{1}}{\rm{.129}}} $$

(11)

• redshank:

$$ {\rm{DEE = 1}}{\rm{.549 }}M^{{\rm{1}}{\rm{.092}}} $$

(12)

No predictions of ME and RI were made at ages 0−2 days, because regression equations overestimate energy requirements during this period (there is a rapid increase in metabolism over the first 3 days, Visser and Ricklefs 1993), and because the contribution of energy stores present in the hatchling (yolk) was not taken into account.

The effect of environmental and physiological variables on FT and RI was explored by exchanging environment and species parameters. For instance, a redshank chick was virtually transposed into the Arctic by changing daylength from 16 to 24 h/day and T _e from 15°C to 3°C. Subsequently exchanging Eq. 4 for Eq. 3 shows the effect on foraging time of a knot's greater cold-hardiness than that of a redshank.

When comparing ME and RI between the species, the difference in growth rate must be taken into account, as ME depends strongly on body mass. We did so by inserting the red knot growth equation, (Eq. 1) into the model for common redshank. Klaassen and Drent (1991) proposed that Resting Metabolic Rate in hatchling birds is coupled to growth rate, which implies that redshank could only grow at a knot's rate at the expense of an increase in RMR. A rough estimate of this additional effect would be a 9% increase of ME (based on Fig. 4 in Klaassen and Drent 1991, a 75% higher growth rate would lead to a 29% increase in RMR which is c. 33% of ME in temperate shorebird chicks, Schekkerman and Visser 2001).