Joseph B. Williams

Tropical birds have a slow pace of life

Tropical birds are relatively long-lived and produce few offspring, which develop slowly and mature relatively late in life, the slow end of the life-history axis, whereas temperate birds lie at the opposite end of this continuum. We tested the hypothesis that tropical birds have evolved a reduced basal metabolic rate (BMR). We measured BMR of 69 species of tropical birds, the largest data set amassed on metabolic rates of tropical birds, and compared these measurements with 59 estimates of BMR for temperate birds. Our analyses included conventional least squares regression, regressions based on phylogenetic independent contrasts, and a comparison of BMR of 13 phylogenetically matched pairs, one species from the tropics and one from northerly temperate areas. Our triptych showed that tropical birds had a reduced BMR, compelling evidence for a connection between the life history of tropical birds and a slow pace of life. Further, tropical migrants breeding in temperate habitats had a lower BMR than did temperate residents, suggesting that these migrants have physiological traits consistent with a slow pace of life. In addition, we determined that tropical birds had a lower cold-induced peak metabolic rate and thermogenic metabolic scope than temperate species, a finding that is consistent with the hypothesis that their environment has not selected for high levels of thermogenesis, or alternatively, that a slow pace of life may be incompatible with high thermogenic capacity. We conclude that physiological function correlates with the suite of life-history traits.

Constitutive innate immunity is a component of the pace-of-life syndrome in tropical birds

We studied the relationship between one component of immune function and basal metabolic rate (BMR), an indicator of the ‘pace-of-life syndrome’, among 12 tropical bird species and among individuals of the tropical house wren (Troglodytes aedon), to gain insights into functional connections between life history and physiology. To assess constitutive innate immunity we introduced a new technique in the field of ecological and evolutionary immunology that quantifies the bactericidal activity of whole blood. This in vitro assay utilises a single blood sample to provide a functional, integrated measure of constitutive innate immunity. We found that the bactericidal activity of whole blood varied considerably among species and among individuals within a species. This variation was not correlated with body mass or whole-organism BMR. However, among species, bacteria killing activity was negatively correlated with mass-adjusted BMR, suggesting that species with a slower pace-of-life have evolved a more robust constitutive innate immune capability. Among individuals of a single species, the house wren, bacteria killing activity was positively correlated with mass-adjusted BMR, pointing to physiological differences in individual quality on which natural selection potentially could act.

The Adjustment of Avian Metabolic Rates and Water Fluxes to Desert Environments

We tested the hypothesis that birds in arid environments, where primary productivity is low and surface water is scarce, have reduced energy expenditure and water loss compared with their mesic counterparts. Using both conventional least squares regression and regression based on phylogenetically independent contrasts, we showed that birds from desert habitats have reduced basal and field metabolic rates compared with species from mesic areas. Previous work showed that desert birds have reduced rates of total evaporative water loss when exposed to moderate environmental temperatures in the laboratory. We tested whether reduced rates of total evaporative water loss translate into low field water fluxes. Conventional ANCOVA indicated that desert birds have reduced water fluxes, but an analysis based on phylogenetically independent contrasts did not support this finding, despite the wide array of taxonomic affiliations of species in the data set. We conclude that the high ambient temperatures, the low primary productivity, and the water scarcity in desert environments have selected for or resulted in reduced rates of energy expenditure and evaporative water loss in birds that live in these climes.

Variability in feeding rate and meal size of Leach's storm-petrel at Kent Island, New Brunswick

(1) Feeding rate and meal size of Leachs storm-petrel at Kent Island, New Brunswick, were studied by analysing mass increments of the chicks. (2) Meal size, estimated by mass increments over short periods during the night, averaged 10.0 g (S.D. = 2.3 g, range approximately 5-13 g). (3) Mass increments over 24 h (NET) were linearly related to the sum of positive mass increments over 3-h intervals during the night (SUM) by the equation NET = -6.04 + 0.92 SUM (r2 = 0.88). With knowledge of meal size and of this relationship, we estimated the number of feeds per night (0, 1, or 2) from NET. (4) During August in both 1962 and 1983, each parent fed its chick on 43% of nights. Each parent fed independently of the other. Percentages of nights with 0, 1, and 2 feeds were 35, 44, and 21%, which do not differ significantly from the binomial probability function with P = 0.43. (5) The probability of a parent feeding its chick (p) did not vary with respect to date (i) in 1983. In 1962, P, was significantly below average on 3 nights and above average on 3 nights. Periods between feeds by either or both parents were 57% = 1 day, 31% = 2 days, and 11% = 3 days in 1983, and 45%, 43%, 9%, 2% (4 days), and 1% (5 days) in 1962. (6) We estimated that intervals between feedings by an individual parent were 22% = 1 day, 38% = 2 days, 23% = 3 days, and 17% = 4 days in 1983. Meal size was independent of the number of days since the previous feeding. (7) After removing variation attributable to date in season (hence age) and difference between chicks, variance in chick mass was 47.8 g2. This was approximately equal to the variance in NET (51.6 g2), indicating that short-term variance in chick mass is generated anew each night by variation in amount fed. Furthermore, the covariance between NET on one night and the next is negative and about half the value of the variance, demonstrating short-term regulation of food delivery. (8) Variability in feeding rate and meal size indicates that intervals between feeds rarely are so long as the period over which chicks could survive utilizing only their substantial fat reserves. This calls into question the prevalent idea that the purpose of the fat deposits is to guarantee survival through periodic fasts resulting from unpredictable food supplies or feeding conditions. Furthermore, food provisioning in storm-petrels appears to be regulated by the requirements of the chicks, rather than by variation in food resources available to adults.

Phenotypic variation of larks along an aridity gradient: Are desert birds more flexible?

We investigated interindividual variation and intra-individual phenotypic flexibility in basal metabolic rate (BMR), total evaporative water loss (TEWL), body temperature (Tb), the minimum dry heat transfer coefficient (h), and organ and muscle size of five species of larks geographically distributed along an aridity gradient. We exposed all species to constant environments of 15°C or 35°C, and examined to what extent interspecific differences in physiology can be attributed to acclimation. We tested the hypothesis that birds from deserts display larger intra-individual phenotypic flexibility and smaller interindividual variation than species from mesic areas. Larks from arid areas had lower BMR, TEWL, and h, but did not have internal organ sizes different from birds from mesic habitats. BMR of 15°C-acclimated birds was 18.0%, 29.1%, 12.2%, 25.3%, and 4.7% higher than of 35°C-acclimated Hoopoe Larks, Dunns Larks, Spike-heeled Larks, Skylarks, and Woodlarks, respectively. TEWL of 15°C-acclimated Hoopoe Larks exceeded values for 35°C-acclimated individuals by 23% but did not differ between 15°C- and 35°C-acclimated individuals in the other species. The dry heat transfer coefficient was increased in 15°C-acclimated individuals of Skylarks and Dunns Larks, but not in the other species. Body temperature was on average 0.4°C ± 0.15°C (mean ± 1 sem) lower in 15°C-acclimated individuals of all species. Increased food intake in 15°C-acclimated birds stimulated enlargement of intestine (26.9–38.6%), kidneys (9.8–24.4%), liver (16.5–27.2%), and stomach (22.0–31.6%). The pectoral muscle increased in 15°C-acclimated Spike-heeled Larks and Skylarks, remained unchanged in Hoopoe Larks, and decreased in 15°C-acclimated Woodlarks and Dunns Larks. We conclude that the degree of intra-individual flexibility varied between physiological traits and among species, but that acclimation does not account for interspecific differences in BMR, TEWL, and h in larks. We found no general support for the hypothesis that species from desert environments display larger intra-individual phenotypic flexibility than those from mesic areas. The coefficient of variation of larks acclimated to their natural environment was smaller in species from arid areas than in species from mesic areas for mass-corrected BMR and surface-specific h, but not for mass-corrected TEWL. The high repeatabilities of BMR, TEWL, and h in several species indicated a within-individual consistency on which natural selection could operate.

A PHYLOGENETIC PERSPECTIVE OF EVAPORATIVE WATER LOSS IN BIRDS

Allometry, the study of the consequences of body size on form and function, has been a powerful investigative tool in avian biology. Comparison of phenotypic data with allometric reference equations permits the identification of possible adaptations and the formulation of hypotheses for testing. The standard allometric equation that relates total evaporative water loss (TEWL) to body mass in birds, published more than two decades ago, was based on a relatively small sample size, and was constructed using procedures which may have biased parameter estimation. In this report, I have analyzed data for TEWL for 102 species of birds ranging in size from hummingbirds to Ostriches (Struthio camelus) using both least-squares regression and phylogenetically independent contrasts. Both approaches suggest that: (1) the slope of the relationship between TEWL and body mass is higher than the value originally proposed; (2) birds from arid environments have a statistically lower TEWL than do birds from more mesic environments; and (3) small birds have similar ratios of TEWL to oxygen consumed compared to larger species. The latter finding negates the idea that small desert birds replenish proportionately less of their TEWL with metabolic water than do larger species. Received 19 June 1995, accepted 22 September 1995.

The control of the balance between ceramide and sphingosine-1-phosphate by sphingosine kinase: oxidative stress and the seesaw of cell survival and death.

Sphingolipids are components of all eukaryotic cells that play important roles in a wide variety of biological processes. Ceramides and sphingosine-1-phosphate (S1P) are signaling molecules that regulate cell fate decisions in a wide array of species including yeast, plants, vertebrates, and invertebrates. Ceramides favor anti-proliferative and cell death pathways such as senescence and apoptosis, whereas S1P stimulates cell proliferation and survival pathways. The control of cell fate by these two interconvertible lipids has been called the sphingolipid rheostat or sphingolipid biostat. Sphingosine kinase, the enzyme that synthesizes S1P, is a crucial enzyme in regulation of the balance of these sphingolipids. Sphingosine kinase has been shown to play dynamic roles in the responses of cells to stress, leading to modulation of cell fate through a variety of signaling pathways impinging on the processes of cell proliferation, apoptosis, autophagy and senescence. This review summarizes the roles of sphingosine kinase signaling in these processes and the mechanisms mediating these responses. In addition, we discuss the evidence tying sphingosine kinase-mediated stress responses to the process of aging.

Interspecific associations between circulating antioxidant levels and life-history variation in birds

Antioxidants play an important role in protecting tissues against aging‐associated oxidative damage and are thus prime candidates for relating physiological mechanisms to variation in life histories. We measured total antioxidant capacity, antioxidant response to stress, and levels of uric acid, vitamin E, and four carotenoids in 95 avian species, mostly passerines from Michigan or Panama. We compared antioxidant measures to seven variables related to life histories (clutch size, survival rate, incubation period, nestling period, basal metabolic rate, body mass, and whether the species lived in a tropical or temperate climate). Life‐history‐related traits varied over at least three statistically independent axes. Higher antioxidant levels were generally characteristic of more rapid development, lower survival rate, smaller body size, larger clutch size, and higher mass‐adjusted metabolic rate, but the relationships of particular antioxidants with individual life‐history traits showed considerable complexity. Antioxidant–life history associations differed between tropical and temperate species and varied with respect to taxonomic sampling. Vitamin E showed few relationships with life‐history traits. Overall, our results partly support the hypothesis that antioxidant levels evolve to mirror free radical production. Clearly, however, the complex patterns of physiological diversification observed here result from the interplay of many factors, likely including not just investment in somatic maintenance but also phylogenetic constraint, diet, and other aspects of ecology.

Basal Metabolic Rate in Carnivores Is Associated with Diet after Controlling for Phylogeny

Studies of basal metabolic rate (BMR), the minimum metabolic rate of postabsorptive, inactive endotherms while in their rest phase and thermal neutral zone, have contributed significantly to our understanding of animal energetics. Besides body mass, the main determinant of BMR, researchers have invoked diet and phylogenetic history as important factors that influence BMR, although their relative importance has been controversial. For 58 species within the Carnivora, we tested the hypothesis that BMR is correlated with home range size, a proxy for level of activity, and diet, using conventional least squares regression (CLSR) and regression based on phylogenetic independent contrasts (PIC). Results showed that BMR of Carnivora was positively correlated with home range size after controlling for body mass, regardless of the statistical method employed. We also found that diet and mass‐adjusted home range size were correlated. When we simultaneously tested the effect of diet and mass‐adjusted home range on mass‐adjusted BMR, home range size was insignificant because of its colinearity with diet. Then we eliminated home range size from our model, and diet proved to be significant with both CLSR and PIC. We concluded that species that eat meat have larger home ranges and higher BMR than species that eat vegetable matter. To advance our understanding of the potential mechanisms that might explain our results, we propose the “muscle performance hypothesis,” which suggests that selection for different muscle fiber types can account for the differences in BMR observed between meat eaters and vegetarian species within the Carnivora.

Physiological Adaptation in Desert Birds

Abstract We call into question the idea that birds have not evolved unique physiological adaptations to desert environments. The rate at which desert larks metabolize energy is lower than in mesic species within the same family, and this lower rate of living translates into a lower overall energy requirement in the wild. We argue that selection has reduced oxygen consumption at the tissue level under basal conditions for birds living in deserts. We document that total evaporative water loss—the sum of cutaneous water loss (CWL) and respiratory water loss—is reduced in desert birds, and present evidence that changes in CWL are responsible for this pattern. The diminution in CWL is attributable to changes in the lipid structure of the stratum corneum of the skin, the physical barrier to diffusion of water vapor. Finally, we show linkages between physiology and life-history attributes of larks along an aridity gradient; birds from deserts have not only a reduced rate of metabolism but also a small clutch size and slow nestling development. Hence, attributes of physiology are correlated with traits that directly affect reproductive success. Our hope is that we will prompt students to question the notion that birds do not possess physiological adaptations to the desert environment, and raise the specter of doubt about “preadaptation” in birds living in deserts.