Maurine W. Dietz

Empirical evidence for differential organ reductions during trans–oceanic bird flight

Since the early 1960s it has been held that migrating birds deposit and use only fat as fuel during migratory flight, with the non–fat portion of the body remaining homeostatic. Recent evidence from field studies has shown large changes in organ sizes in fuelling birds, and theory on fuel use suggests protein may be a necessary fuel during flight. However, an absence of information on the body condition of migrants before and after a long flight has hampered understanding of the dynamics of organs during sustained flight. We studied body condition in a medium–sized shorebird, the great knot (Calidris tenuirostris), before and after a flight of 5400 km from Australia to China during northward migration. Not only did these birds show the expected large reduction in fat content after migration, there was also a decrease in lean tissue mass, with significant decreases in seven organs. The reduction in functional components is reflected in a lowering of the basal metabolic rate by 46%. Recent flight models have tried to separate the ‘flexible’ part of the body from the constant portion. Our results suggest that apart from brains and lungs no organs are homeostatic during long–distance flight. Such organ reductions may be a crucial adaptation for long–distance flight in birds.

Glutamate phase shifts circadian activity rhythms in hamsters

The suprachiasmatic nuclei (SCN) have been identified as a pacemaker for many circadian rhythms in mammals. Photic entrainment of this pacemaker can be accomplished via the direct retino-hypothalamic tract (RHT). Glutamate is a putative transmitter of the RHT. In the present study it is demonstrated that glutamate injections in the SCN cause phase shifts of the circadian activity rhythm of the hamster. In contrast, glutamate injections outside the SCN or vehicle injections inside the SCN did not affect the circadian phase. These data suggest that glutamate could be involved in photic entrainment of the circadian pacemaker.

Parental energy expenditure during brood rearing in the Great Tit (Parus major) in relation to body mass, temperature, food availability and clutch size

1. Quantification of the energetic needs of reproducing animals provides a basis for understanding patterns in reproduction. The doubly labelled water technique enables this to be carried out under natural conditions. 2. Daily energy expenditure of 32 female Great Tits (Parus major) tending nestlings 11-12 days old (DEE(par)) and energy expenditure at night of five females was measured using the doubly labelled water technique. 3. Average DEE(par) was 95.1 kJ (24 h)-1 (1.10 W) and close to most predictions based on interspecific allometric relationships. Night metabolism was estimated to be 0.68 W. 4. Individual variation in DEE(par) could be explained by variation in body mass (+), ambient temperature (-), clutch size (+) and food availability (-) but not by female tarsus length, age, brood size or nestling mass. The significant factors together accounted for the differences found between years and broods and explained 64% of the variation. Possible causal pathways are discussed. 5. The DEE(par) in Great Tits was related to body mass with an exponent of 1.99; significantly steeper than the interspecific exponent of 0.67-0.75 reported in the literature. Analysis of intraspecific variation in DEE(par) for 10 species tending young, revealed variable trends with body mass.

Is Long‐Distance Bird Flight Equivalent to a High‐Energy Fast? Body Composition Changes in Freely Migrating and Captive Fasting Great Knots

We studied changes in body composition in great knots, Calidris tenuirostris, before and after a migratory flight of 5,400 km from northwest Australia to eastern China. We also took premigratory birds into captivity and fasted them down to their equivalent arrival mass after migration to compare organ changes and nutrient use in a low‐energy‐turnover fast with a high‐energy‐turnover fast (migratory flight). Migrated birds were as economical as any fasting animal measured yet at conserving protein: their estimated relative protein contribution (RPC) to the energy used was 4.0%. Fasted birds had an estimated RPC of 6.8% and, consequently, a much lower lean mass and higher fat content for an equivalent body mass than migrated birds. Lean tissue was catabolized from most organs in both groups, except the brain. Furthermore, a principal components biplot showed that individuals were grouped primarily on the basis of overall organ fat or lean tissue content rather than by the size of specific organs. This indicates that organ changes during migratory flight are similar to those of a low‐energy fast, although the length of the fast in this study probably accentuated organ reductions in some functional groups. Whether the metabolic characteristics of a flying migratory fast follow the three‐phase model described in many inactive fasting animals is unclear. We have some evidence for skeletal fat being catabolized without phase 3 of a fast having been reached.

Estimating organ size in small migrating shorebirds with ultrasonography : An intercalibration exercise

Organs, even of fully grown adult birds, mammals, and reptiles, may show substantial size changes in relation to specific performances. These changes are difficult to study, because measurements usually can only be obtained following the death of the animal. We explored the use of ultrasonographic imaging, a relatively simple noninvasive technique, to measure size of pectoral muscles and stomach in two small shorebird species (red knots Calidris canutus and golden plovers Pluvialis apricaria). Accuracy of ultrasound measurements in estimating organ mass in red knots was reasonably high. Depending on the equipment used, the error of individual measurements was 20%–25% for the pectoral muscles and 26%–44% for the stomach. In plovers the technique was less accurate, probably because of the low variability of the organs involved. Ultrasound scanning is particularly suited to measure rapidly changing organ sizes over short time intervals. We demonstrate this with an example in which changes in individuals in size of pectoral muscle and stomach were monitored in captive red knots following a change in diet. Ultrasound measures will enable studies on the links between body composition and future behavior and physiology.

ENERGY-REQUIREMENTS FOR MOLT IN THE KESTREL FALCO-TINNUNCULUS

We estimated energy requirements for plumage replacement in the kestrel (Falco tinnunculus) by comparing O₂, consumption V̇o2 and metabolizable energy intake during molt and nonmolt. The energy expenditure for feather synthesis (S) as derived from the regression of basal metabolic rate (BMR) on molt intensity was 104 kJ·(g dry feathers)⁻¹. As derived from the regression of the resting metabolic rate of nonfasting birds at night (RMR) on molt intensity, S was 108 kJ·g⁻¹, and statistically indistinguishable from the BMR estimate. During the first part of molt the coefficient of temperature dependence of the standard metabolic rate below thermoneutrality (SMR) increased from 0.050 to 0.070 W·° C⁻¹. The metabolizable energy required for maintenance (Mm) increased with increasing body mass. The Mm in males was higher than in females of the same body mass. The Mm during molt was higher than during nonmolt episodes. The estimate for the cost of feather synthesis based on this difference was S = 117 kJ·g⁻¹. The cost of feather synthesis in the kestrel is thus much lower than values reported for three passerines (230-835 kJ·g⁻¹). This difference in efficiency may be related to diet (carnivorous vs. granivorous birds) or body mass.

The Effects of Intraventricular Carbachol Injections on the Free-Running Activity Rhythm of the Hamster

The effects of light on the circadian pacemaker in the suprachiasmatic nucleus (SCN) are mediated by the retinohypothalamic tract (RHT) and by the retinogeniculosupra chiasmatic tract (RGST). The neurotransmitter of the RGST is neuropeptide Y. The RHT may contain glutamate and aspartate. Recent evidence indicates that acetylcholine could also be involved in phase shifting by light. We determined that intraventricular injections with an acetylcholine agonist, carbachol, induces phase advances during the subjective day and phase delays during the early subjective night. No differences were observed between phase shifts induced in constant darkness and those induced in continuous light. A dose-response curve for carbachol was described at circadian time 6 (CT6). Injections at CT14 with various dosages of carbachol indicated the same dose dependency for this circadian time. Finally, carbachol injections in split animals resulted in similar responses of the two components of the split activity rhythm.

Basal Metabolic Rate Declines During Long-Distance Migratory Flight in Great Knots

Abstract Great Knots (Calidris tenuirostris) make one of the longest migratory flights in the avian world, flying almost 5500 km from Australia to China during northward migration. We measured basal metabolic rate (BMR) and body composition in birds before and after this flight and found that BMR decreased 42%. The mass-specific BMR based on lean mass decreased 33%. We also starved a group of pre-migratory Great Knots in captivity to determine whether they showed the same reduction in BMR without having undergone the hard work of flight. The captive birds showed a similar range and reduction of BMR values as the wild birds. Exponents of relationships between BMR and body mass in different comparisons were high, indicating large changes in BMR as a function of body mass. Analysis of the body composition of ten wild and three captive birds found that the flight muscle mass and intestine mass positively correlated with BMR. La Tasa Metabolica Basal Disminuye durante Vuelos Migratorios de Larga Distancia en Calidris tenuirostris Resumen. Calidris tenuirostris realiza uno de los vuelos migratorios más largos entre las aves, volando desde Australia hasta China durante la migración al norte. Medimos la tasa metabólica basal (TMB) y la composición corporal en aves antes y después del vuelo y encontramos que TMB se reduce en 42%. La TMB específica por masa, o sea la TMB corregida por masa magra, se redujo en 33%. También expusimos un grupo premigratorio de Calidris tenuirostris a un periodo de ayuno en cautiverio, para determinar si mostraban una tasa de reducción similar en la TMB sin haber soportado la dura tarea de volar. Las aves en cautiverio mostraron un rango y una reducción de los valores de la TMB similares a los de las aves en libertad. Los exponentes de la relación entre TMB y masa corporal en diferentes comparaciones fueron altos, indicando grandes cambios de la TMB en función de la masa corporal. El análisis de la composición corporal de diez aves libres y tres en cautiverio mostró que la masa de los músculos del vuelo y la masa de los intestinos esta positivamente correlacionada con la TMB.

Daily energy budgets of avian embryos: The paradox of the plateau phase in egg metabolic rate

The metabolic rate of precocial bird eggs reaches a plateau when about 80% of the incubation period has passed. This is unexpected, as in many species the embryo continues to grow and maintenance costs must therefore increase. To investigate this paradox, daily energy budgets were constructed for embryos of four galliform species according to two models that used empirical data on egg metabolic rate and embryo growth. In the first model, embryonic synthesis costs were estimated, with an assumed synthesis efficiency, before calculating the maintenance costs. In the second model, embryonic maintenance was calculated first, and no assumptions were made on the synthesis efficiency. The calculations show that assumptions of the synthesis efficiency had a major impact on the energy budget calculations, because embryonic growth rate was high. During the plateau phase, a galliform embryo allocated energy in favor of its maintenance costs in three ways: by decreasing growth rate, by increasing synthesis efficiency, and by depressing the formation of glycogen. Our study suggests that a reduction in growth rate plays a minor role. An increase of synthesis efficiency is more likely to explain the plateau in energy expenditure, since small increases in synthesis efficiency can lead to great savings on synthesis costs.

Heat Increment of Feeding in the Kestrel, Falco tinnunculus, and its Natural Seasonal Variation

We measured the Heat Increment of Feeding (H) as the difference in oxygen consumption between the fed and fasting state in the kestrel at different ambient temperatures. Total H is a constant fraction of metabolizable energy intake and amounts to 16.6% of the energy assimilated. The effect of a meal was detected as elevation in metabolic rate lasting until 20 hours after the meal, independently of meal size. Below thermoneutral temperatures only part of H compensates for the cost of thermoregulation (T) up to a reallocation of 50% of H to T. Even at low temperatures (-12 °C) metabolic rate of fed kestrels is thus higher than that of fasting birds.