Clade-Specific Allometries in Avian Basal Metabolic Rate Demand a Broader Theory of Allometry.

AbstractMany attempts at providing a single-scale exponent and mechanism to explain metabolic rate assert a monolithic selective mechanism for allometries, characterized by a universal allometric scale power (usually chosen to be 0.75). To test for the deviations from universal allometric scaling, we gathered data from previously published metabolic measurements on 903 bird species and performed regressions of log(basal metabolic rate) and log(body mass) for (1) all birds and (2) 20 monophyletic clades within birds. We constructed two Bayesian linear mixed models-one included ecological variables and the other included data for mammals from Sieg et al. (2009). Overall allometric patterns differed significantly among clades of birds, and some clades were not consistent with the 0.75 scale power. We were unable to find apparent physiological, morphological, phylogenetic, or ecological characteristics among clades, predicting a difference in allometry or consistency with any previously proposed universal allometry. The Bayesian analysis illuminated novel bivariate, clade-specific differences in scaling slope-intercept space, separating large groups of birds and mammals. While significantly related to basal metabolic rate, feeding guild and migratory tendency had small effects compared to clade and body mass. We propose that allometric hypotheses, in general, must extend beyond simple overarching mechanisms to allow for conflicting and interacting influences that produce allometric patterns at narrower taxonomic scales-perhaps including other processes whose optimization may interfere with that of the system proposed by the metabolic theory of ecology.

Mammalian metabolic allometry: do intraspecific variation, phylogeny, and regression models matter?

Power scaling relationships between body mass and organismal traits are fundamental to biology. Compilations of mammalian masses and basal metabolic rates date back over a century and are used both to support and to assail the universal quarter-power scaling invoked by the metabolic theory of ecology. However, the slope of this interspecific allometry is typically estimated without accounting for intraspecific variation in body mass or phylogenetic constraints on metabolism. We returned to the original literature and culled nearly all unique measurements of body mass and basal metabolism for 695 mammal species and (1) phylogenetically corrected the data using the fullest available phylogeny, (2) applied several different regression analyses, (3) resampled regressions by drawing randomly selected species from each of the polytomies in the phylogenetic hypothesis at each iteration, and (4) ran these same analyses independently on separate clades. Overall, 95% confidence intervals of slope estimates frequently did not include 0.75, and clade-specific slopes varied from 0.5 to 0.85, depending on the clade and regression model. Our approach reveals that the choice of analytical model has a systematic influence on the estimated allometry, but irrespective of the model applied, we find little support for a universal metabolic rate-body mass scaling relationship.

Phylogeny, regression, and the allometry of physiological traits.

Physiological and ecological allometries often pose linear regression problems characterized by (1) noncausal, phylogenetically autocorrelated independent (x) and dependent (y) variables (characters); (2) random variation in both variables; and (3) a focus on regression slopes (allometric exponents). Remedies for the phylogenetic autocorrelation of species values (phylogenetically independent contrasts) and variance structure of the data (reduced major axis [RMA] regression) have been developed, but most functional allometries are reported as ordinary least squares (OLS) regression without use of phylogenetically independent contrasts. We simulated Brownian diffusive evolution of functionally related characters and examined the importance of regression methodologies and phylogenetic contrasts in estimating regression slopes for phylogenetically constrained data. Simulations showed that both OLS and RMA regressions exhibit serious bias in estimated regression slopes under different circumstances but that a modified orthogonal (least squares variance-oriented residual [LSVOR]) regression was less biased than either OLS or RMA regressions. For strongly phylogenetically structured data, failure to use phylogenetic contrasts as regression data resulted in overestimation of the strength of the regression relationship and a significant increase in the variance of the slope estimate. Censoring of data sets by simulated extinction of taxa did not affect the importance of appropriate regression models or the use of phylogenetic contrasts.

Linking physiological effects on activity and resource use to population level phenomena.

We present an approach to delineating physiological effects on population level processes by modeling the activity and resource budgets of animals. Physiology and its environmental forcing functions are assumed to affect both the total time available for activity and foraging and the resource budgets by affecting resource acquisition, costs, and handling. We extend the earlier model of Dunham and others (1989) and translate it into a computational algorithm. To satisfy conservation needs for accuracy, wide applicability, and rapid deployment, the model is relatively simple, uses as much data on the focal organism as possible, is mechanistically driven, and can be adapted to new organisms by using data for the new species, or the best available approximations to those data. We present 2 applications of the modeling approach. First, we consider a system with substantial information available, canyon lizards (Sceloporus merriami) studied by Dunham and colleagues in west Texas. In this case the focus is on integration of numerous inputs and the ability of the model to produce predictions that approximate counterintuitive empirical patterns. By using the wealth of specific data available, the model outperforms previous attempts at explanation of those patterns. Next, we consider a system with much less available information (forest-dwelling semi-fossorial frogs). The question here is how hydric conditions can become limiting. A model of evaporation from frogs buried in leaf litter was incorporated and it demonstrates how rainfall patterns can both supply water and put the frogs at risk of critical dehydration.

Bergmann's Clines in Ectotherms: Illustrating a Life-History Perspective with Sceloporine Lizards.

The generality and causes of Bergmann's rule have been debated vigorously in the last few years, but Bergmann's clines are rarely explained in the context of life-history theory. We used both traditional and phylogenetic comparative analyses to explore the causes of latitudinal and thermal clines in the body size of the eastern fence lizard (Sceloporus undulatus). The proximate mechanism for larger body sizes in colder environments is delayed maturation, which results in a greater fecundity but a lower survival to maturity. Life-history theory predicts that a higher survivorship of juveniles in colder environments can favor the evolution of a Bergmann's cline. Consistent with this theory, lizards in colder environments survive better as juveniles and delay maturation until reaching a larger body size than that of lizards in warmer environments. We expect similar relationships among temperature, survivorship, and age/size at maturity exist in other ectotherms that exhibit Bergmann's clines. However, life-history traits of S. undulatus were more strongly related to latitude than they were to temperature, indicating that both abiotic and biotic factors should be considered as causes of Bergmann's clines. Nonetheless, analyses of the costs and benefits of particular body sizes in different thermal environments will enhance our understanding of geographic variation.

The temperature-size rule in ectotherms: simple evolutionary explanations may not be general.

In many organisms, individuals in colder environments grow more slowly but are larger as adults. This widespread pattern is embodied by two well-established rules: Bergmann's rule, which describes the association between temperature and body size in natural environments, and the temperature-size rule, which describes reaction norms relating temperature to body size in laboratory experiments. Theory predicts that organisms should grow to be larger in colder environments when growth efficiency decreases with increasing environmental temperature. Using data from 97 laboratory experiments, including 58 species of ectotherms, we found little evidence that growth efficiency is negatively related to environmental temperature within the thermal range that is relevant to the temperature-size rule. Instead, growth efficiency was either positively related or insensitive to environmental temperature in the majority of cases (73 of 89 cases for gross growth efficiency and 18 of 24 cases for net growth efficiency). Two possibilities merit consideration. First, high temperatures may impose constraints on growth that only arise late during ontogeny; this simple and potentially general explanation is supported by the fact that thermal optima for growth efficiency and growth rate decrease as individuals grow. Alternatively, the general explanation for relationships between temperature and body size may not be simple. If the latter view is correct, the best approach might be to generate and test theories that are tailored specifically to organisms with similar behavior and physiology.

Clinical features and outcome in dogs and cats with obsessive-compulsive disorder: 126 cases (1989-2000).

OBJECTIVE: To determine clinical features and outcome in dogs and cats with obsessive-compulsive disorder (OCD). DESIGN: Retrospective study. ANIMALS: 103 dogs and 23 cats. PROCEDURES: Records of patients with OCD were analyzed for clinical features, medication used, extent of behavior modification, and outcome. RESULTS: Most dogs affected with OCD had been obtained from breeders. Male dogs significantly outnumbered females (2:1). Female cats outnumbered male cats by 2:1 in a small sample. Most affected dogs lived in households with 2 or more humans and other dogs or cats, and had some formal training. Client compliance with behavior modification was high. A combination of behavior modification and medication resulted in a large decrease in intensity and frequency of OCD in most animals. Clomipramine was significantly more efficacious for treatment in dogs than was amitriptyline. Only 1 dog and 1 cat were euthanatized because of OCD during the study. CONCLUSIONS AND CLINICAL RELEVANCE: OCD in dogs does not appear to be associated with lack of training, lack of household stimulation, or social confinement. In cats, OCD may be associated with environmental and social stress. Obsessive-compulsive disorder appears at the time of social maturity and may have sporadic and heritable forms. With appropriate treatment (consistent behavior modification and treatment with clomipramine), frequency and intensity of clinical signs in most dogs and cats may decrease by > 50%. Success appears to depend on client understanding and compliance and the reasonable expectation that OCD cannot be cured, but can be well controlled.

The relationship of body size to survivorship of hatchling snapping turtles (Chelydra serpentina): an evaluation of the "bigger is better" hypothesis.

In many organisms, body size is positively correlated with traits that are presumably related to fitness. If directional selection frequently favors larger offspring (the "bigger is better" hypothesis), the results of such selection should be detectable with field experiments. We tested the "bigger is better" hypothesis in hatchling snapping turtles (Chelydra serpentina) by conducting one long-term and three short-term experiments on the University of Michigan E.S. George Reserve in southeastern Michigan. In the fall of 1995 and 1996, we released hatchlings at artificial nests separated from the nearest wetland by fences. We recorded the proportion of hatchlings recaptured, the time it took hatchlings to move to fences from artificial nests 45, 55, and 80 m away, and dispersion along the fence. We determined whether the response variables and probability of recapture at fences were associated with hatchling body size. During 1995, average travel times of hatchlings from the experimental nests were not related to distance from the fence; however, time to recapture was positively correlated with dispersion from the zero point on the fence, and the maximum time to reach the fence was almost twice as long for hatchlings from the 80-m nest compared to those from the 45-m nest. Sixty-seven percent of the hatchlings reached the fence and the proportions doing so from each nest were not different. Body size was not significantly related to probability of recapture in either of the 1995 experiments. In 1996, 59% of released hatchlings were recaptured. Time to recapture was not related to dispersion from the zero point or to body size. Cubic spline analysis suggested stabilizing selection on body size. We also conducted a set of long-term hatchling release experiments between 1980-1993 to compare the survival of hatchlings released at nest sites to that of hatchlings released directly into marshes, and we looked for relationships between survivorship and hatchling body size. During 7 years in which more than 30 hatchlings were released, 413 hatchlings were released directly into the marsh and 262 were released at nests: their probability of survival did not differ. Over all years, for both release groups combined and for each group separately, survival was not related to body size. In 1983 alone, survival was also not related to body size for either group or for both groups combined. In our three short-term experiments and one long-term experiment, we found no evidence to support the "bigger is better" hypothesis. When selection on body size did occur, selection was stabilizing, not directional for larger size.

EFFECTS OF MORTALITY RISK AND GROWTH ON A MODEL OF REPRODUCTIVE EFFORT: WHY THE SHINE AND SCHWARZKOPF MODEL IS NOT GENERAL.

Using data and reanalysis of a model published by Shine and Schwarzkopf (1992) we reject the two unsubstantiated assertions made by Shine et al. (1996) about modeling the evolution of reproductive effort in squamate reptiles: (1) mortality schedules do not affect predictions of the Shine and Schwarzkopf (1992) model; and (2) growth rates that would affect the predictions of the original model are biologically unreasonable. On the basis of these two points alone, we strongly reject Shine et al.'s (1996) claim that a critique by Niewiarowski and Dunham (1994) actually reinforces the original conclusions of Shine and Schwarzkopf (1992). Furthermore, results and data presented here are strong enough to severely circumscribe the generality of the Shine and Schwarzkopf (1992) model. Though we do not provide data or new analyses of the potential effects of offspring size variation, we reaffirm the position of Niewiarowski and Dunham (1994) that the sensitivity of the Shine and Schwarzkopf (1992) model to such effects should be explored before using it as a basis for structuring future research on the evolution of reproductive effort in squamate reptiles.

THE PARADOX OF THE PHYLOGENY: CHARACTER DISPLACEMENT OF ANALYSES OF BODY SIZE IN ISLAND ANOLIS.

The evolution of body size in Anolis lizards of the Lesser Antilles Islands has been the subject of intensive, if divisive, study. Early research by Schoener revealed a regularity in the number of Anolis species that coexisted on islands and the difference in body size between coexisting congeners in the Northern Lesser Antilles. This consistent pattern of body size was suggested to be the result of competitive character displacement. Two recent studies critically evaluated this hypothesis by incorporating information about the phylogenetic relationships of insular Anolis. Roughgarden and Pacala suggested that the patterns of body-size differences in the Northern Lesser Antilles could be explained as a cyclical phenomenon that they labeled a taxon cycle. However, Losos supported the character-displacement hypothesis ("size adjustment"). The conflict between these two studies is important because both investigations were based on the same phylogenetic hypothesis. We investigated body-size evolution in Lesser Antilles Anolis to resolve the differences in the conclusions of these studies. Our new analysis supported the taxon-cycle hypothesis but nevertheless failed to reject the character-displacement hypothesis. We argue that this curious scenario is largely a function of the method by which phylogenetic information is incorporated in comparative analyses. Different comparative analyses may lead to dramatic differences in results and ambiguity in the conclusions to be drawn. We suggest that ecologists and evolutionary biologists specifically consider the underlying assumptions and models of character evolution inherent to each of the phylogenetically based analytical methods now available.

THE EVOLUTION OF REPRODUCTIVE EFFORT IN SQUAMATE REPTILES: COSTS, TRADE-OFFS, AND ASSUMPTIONS RECONSIDERED.

We evaluated Shine and Schwarzkopf's (SS) model of the evolution of reproductive effort (RE) in squamate reptiles. They suggested that fecundity trade-offs were unimportant in the evolution of RE in most squamate reptiles and that only survival trade-offs needed to be considered. However, we show that by assuming no variation in offspring size exists, and that adult mortality is episodic, the results of the SS model are not general. By extension, we argue that conclusions drawn about factors important in the evolution of RE in squamate reptiles are premature. Using a modified version of the SS model, we demonstrate that variation in the form of trade-offs relating offspring size and survival substantially affect relationships among clutch size, relative clutch mass, and lifetime reproductive success. We also demonstrate that the way in which adult mortality is simulated drastically affects conclusions about the potential fecundity trade-offs experienced by populations of squamate reptiles. Finally, we suggest that a complete understanding of the evolution of RE will come from theory that incorporates trade-offs between offspring size and quality, as well as other system-specific constraints on the allocation of energy to growth, maintenance, storage, and reproduction.