The functional morphology of the lungs of small Australian passerines having different diurnal activity patterns

Simone Vitali

This thesis examines the relationship between pulmonary microanatomy, metabolic physiology and diurnal activity in Australian passerines. The selected species were sympatric, and were of similar body mass, but differed in the energetic demands of their diurnal routine. The five species selected represented three activity categories: high (Hirundinidae, swallows), moderate (Meliphagidae, honeyeaters) and low (Maluridae, fairy wrens). These classifications were based on literature data, supported by field observation and calculations of flight cost based on measurement of wing morphology. Laboratory metabolism of the five species was quantified by the measurement of standard metabolic rate, and maximal cold-induced metabolic rate. The standard metabolic rates of all except the low activity wrens agreed with allometric predictions for passerine species. The wrens had a significantly lower standard metabolic rate than predicted for passerine species. There was no clear relationship between activity classification and maximal metabolism. The highest maximal metabolic rate was found in the moderately active tawny-crowned honeyeater. The other four species were statistically indistinguishable from one another with regard to this parameter. Maximal metabolic rate was similar across activity categories. The apparent discrepancy in the relationships of standard and maximal metabolism to diurnal activity suggests that standard and maximal metabolism may reflect different anatomical and ecological restrictions. While standard metabolic rate appears to be a good index of daily energetic demand, maximal metabolic rate may reflect the capacity of a species to respond to sudden increases in metabolic demand, such as are associated with fleeing from predators, or sudden changes in atmospheric conditions. Pulmonary anatomy was analysed quantitatively using stereology. Lung volumes, and the proportions of the various lung components discernible at the light microscopy level, were similar in species from all three activity categories. At the ultrastructural level, wrens were found to have a significantly larger plasma volume than the other species. Wrens also had a significantly lower venous haematocrit than the other species. Data derived from stereological analysis were used to calculate diffusing capacities for the various components of the blood-gas barrier, and also the diffusing capacity of the entire lung. These indices were used to quantify the efficiency of oxygen transfer to the erythrocyte. Pulmonary diffusing capacity was significantly lower in the wrens than in the meliphagids and the swallow. The high and moderate activity categories formed a continuum of statistically indistinguishable values. This result reflected laboratory measurements of standard metabolic rate, for which the wren had a significantly lower value than both the meliphagids and the swallow, but the moderate and high activity groups were not significantly different. There was a significant correlation between standard metabolic rate and total pulmonary diffusing capacity (DLO2), and also between venous haematocrit and DLO2. The results indicated that pulmonary anatomy per se is not correlated with field activity or laboratory metabolism. The low pulmonary diffusing capacity of the wren was a product of differences in plasma volume and haematocrit, rather than differences in pulmonary structure as such. The correlation between DLO2 and standard metabolic rate is largely an expression of the effect of haematocrit and plasma volume on DLO2. The results of this study show that the less active wrens have lower standard metabolic rates and lower pulmonary diffusing capacities than the other species. The well developed social hierarchy in wrens and their cooperative breeding behaviour, combined with their energetically inexpensive foraging strategies, may be the ecological basis for their low metabolic rates and pulmonary diffusing capacities. The parameter which appears most significant in effecting low standard metabolic rate and low Dl02 in the wren is its low venous haematocrit.

The functional morphology of the lungs of small Australian passerines having different diurnal activity patterns

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