Negative Allometric Scaling Research Articles

Relative skull size evolution in Mesozoic archosauromorphs: potential drivers and morphological uniqueness of erythrosuchid archosauriforms

AbstractLittle is known about the large‐scale evolutionary patterns of skull size relative to body size, and the possible drivers behind these patterns, in Archosauromorpha. For example, the large skulls of erythrosuchids, a group of non‐archosaurian archosauromorphs from the Early and Middle Triassic, and of theropod dinosaurs are regarded as convergent adaptations for hypercarnivory. However, few investigations have explicitly tested whether erythrosuchid and theropod skulls are indeed disproportionately large for their body size, and whether this trend is driven by hypercarnivory. Here, we investigate archosauromorph relative skull size evolution, examining the scaling relationships between skull and body size of Palaeozoic and Mesozoic archosauromorphs using a robust phylogenetic framework and assessing the influence of potential drivers, such as taxonomy, diet, locomotory mode and inhabited biotope. Our results show that archosauromorph relative skull sizes are largely determined by phylogeny and that the other drivers have much weaker levels of influence. We find negative allometric scaling of skull size with respect to body size when all studied archosauromorphs are analysed. Within specific groups, skull size scales with positive allometry in non‐archosaurian archosauromorphs and, interestingly, scales isometrically in theropods. Ancestral reconstructions of skull–femur size ratio reveal a disproportionately large skull at the base of Erythrosuchidae and proportionately sized skulls at the bases of Theropoda, Carnosauria and Tyrannosauroidea. Relative skull sizes of erythrosuchids and theropods are therefore distinct from each other, indicating that disproportionately large skulls are not a prerequisite for hypercarnivory in archosauromorphs, and that erythrosuchids exhibit a bauplan unique among terrestrial Mesozoic carnivores.

Morphometric and behavioural changes in the early life stages of the sea cucumber Cucumaria frondosa

The present study examined morphological and behavioural development in post-settled juveniles of the commercial sea cucumber Cucumaria frondosa, in an effort to assist captive breeding and conservation initiatives. Juveniles developed all 10 tentacles within 16 months; they had 9 podia and measured 4.6 mm in length after 21 months. Scaling between body length and number of podia was isometric, whereas dorsal tentacle metrics showed negative allometric scaling, indicating that growth was accompanied by a decreasing tentacle to body size ratio. Dorsally-oriented tentacles developed and ramified faster, showing 6 ramifications after 21 months, when ventrally-oriented tentacles only displayed one. This asynchrony underlines the distinctive roles of dorsal vs. ventral tentacles during the early months. The former were strictly used to capture plankton from the water column; whereas the latter were used for anchorage and feeding on deposited material. Ossicles of the body wall increased in length and thickness, and became slightly curved and rounded in older juveniles. Light intensity and water flow tolerance increased with age; from 25 lx and 5 cm s−1 in 1-month-old individuals, to >50 lx and 10 cm s−1 in 6, 12, and 21-month-old individuals, consistent with migration from sheltered to more exposed locations. Moreover, 1 and 6-month-old juveniles preferred rock substrates and black or red background colours; whereas 12 and 21-monthd-old individuals favoured substrates of coralline algae and a red background, also indicative of increasing affinity with sunlit environments and a shift from benthic to planktonic feeding. Juveniles of all age classes were feeding (i.e. had deployed tentacles) 24 h a day and commonly sought vertical surfaces. Together, the findings shed light on the early juvenile ecology of this cold-water suspension-feeding sea cucumber. Considering the expansion of sea cucumber fisheries and growing interest in the aquaculture of C. frondosa, this work also provides a framework for improved stock management and culture protocols.

Dental functional morphology predicts the scaling of chewing rate in mammals

How food intake and mastication scale to satisfy the metabolic needs of mammals has been the subject of considerable scientific debate. Existing theory suggests that the negative allometric scaling of metabolic rate with body mass is compensated by a matching allometric scaling of the chewing rate. Why empirical studies have found that the scaling coefficients of the chewing rate seem to be systematically smaller than expected from theory remains unknown. Here we explain this imparity by decoupling the functional surface area of teeth from overall surface area. The functional surface area is relatively reduced in forms emphasizing linear edges (e.g., lophodont) compared with forms lacking linear structures (e.g., bunodont). In forms with reduced relative functional surface, the deficit in food processed per chew appears to be compensated for by increased chewing rate, such that the metabolic requirements are met. This compensation accounts for the apparent difference between theoretically predicted and observed scaling of chewing rates. We suggest that this reflects adaptive functional evolution to plant foods with different fracture properties and extend the theory to incorporate differences in functional morphology.

Estimating consumable biomass from body length and order in insects and spiders

1. Current models used to estimate insect prey biomass for diet studies use whole weight. However, a large proportion of an arthropod's body is taken up by an indigestible exoskeleton, leading to erroneous estimation of the food intake of insectivorous animals.2. Linear mixed effect models were used to obtain equations to predict consumable biomass from body length for a variety of Neotropical insects and spiders. These data were obtained by feeding taxa of various orders to groups of 100 social spiders and comparing pre‐ and post‐consumption weights using size‐matched controls.3. Significant linear relationships were found relating body size to consumed biomass for all orders, with slopes ranging from 1.276 to 4.011 and R2 values from 0.476 to 0.929. For orders other than spiders and Orthoptera, the increase in weight with size exhibited negative allometric scaling, suggesting a decrease in tissue density, or an increase in internal air space, with size.4. Although there were significant differences across taxonomic orders in the proportion of biomass consumed, within most orders the proportion consumed did not differ significantly with body size. The estimated regression coefficients may be used by other workers to estimate consumable biomass of arthropod prey for studies requiring large sample sizes or non‐lethal sampling of rare or endangered species.

Vertebral bone microarchitecture and osteocyte characteristics of three toothed whale species with varying diving behaviour

Although vertebral bone microarchitecture has been studied in various tetrapods, limited quantitative data are available on the structural and compositional changes of vertebrae in marine mammals. Whales exhibit exceptional swimming and diving behaviour, and they may not be immune to diving-associated bone pathologies. Lumbar vertebral bodies were analysed in three toothed whale species: the sperm whale (Physeter macrocephalus), orca (Orcinus orca) and harbour porpoise (Phocoena phocoena). The bone volume fraction (BV/TV) did not scale with body size, although the trabeculae were thicker, fewer in number and further apart in larger whale species than in the other two species. These parameters had a negative allometric scaling relationship with body length. In sperm whales and orcas, the analyses revealed a central ossification zone (“bone-within-bone”) with an increased BV/TV and trabecular thickness. Furthermore, a large number of empty osteocyte lacunae was observed in the sperm whales. Quantitative backscattered electron imaging showed that the lacunae were significantly smaller and less densely packed. Our results indicate that whales have a unique vertebral bone morphology with an inside-out appearance and that deep diving may result in a small number of viable osteocytes because of diving depth-related osteocyte death.

A potential mechanism for allometric trabecular bone scaling in terrestrial mammals.

Trabecular bone microstructural parameters, including trabecular thickness, spacing, and number, have been reported to scale with animal size with negative allometry, whereas bone volume fraction is animal size-invariant in terrestrial mammals. As for the majority of scaling patterns described in animals, its underlying mechanism is unknown. However, it has also been found that osteocyte density is inversely related to animal size, possibly adapted to metabolic rate, which shows a negative relationship as well. In addition, the signalling reach of osteocytes is limited by the extent of the lacuno-canalicular network, depending on trabecular dimensions and thus also on animal size. Here we propose animal size-dependent variations in osteocyte density and their signalling influence distance as a potential mechanism for negative allometric trabecular bone scaling in terrestrial mammals. Using an established and tested computational model of bone modelling and remodelling, we run simulations with different osteocyte densities and influence distances mimicking six terrestrial mammals covering a large range of body masses. Simulated trabecular structures revealed negative allometric scaling for trabecular thickness, spacing, and number, constant bone volume fraction, and bone turnover rates inversely related to animal size. These results are in agreement with previous observations supporting our proposal of osteocyte density and influence distance variation as a potential mechanism for negative allometric trabecular bone scaling in terrestrial mammals. The inverse relationship between bone turnover rates and animal size further indicates that trabecular bone scaling may be linked to metabolic rather than mechanical adaptations.

Sexual selection, phenotypic variation, and allometry in genitalic and non-genitalic traits in the sexually size-dimorphic stick insectMicrarchus hystriculeus

The mobility hypothesis could explain the evolution of female-biased size dimorphism if males with a smaller body size and longer legs have an advantage in scramble competition for mates. This hypothesis is tested by performing a selection analysis in the wild on Micrarchus hystriculeus (Westwood) (Phasmatodea), a sexually size dimorphic stick insect endemic to New Zealand. This analysis examined the form and strength of sexual selection on body size, leg lengths (front, mid and hind), and clasper size (a genitalic trait), and also quantified the degree of phenotypic variation and the allometric scaling pattern of these traits. By contrast to the mobility hypothesis, three lines of evidence were found to support significant stabilizing sexual selection on male hind leg length: a significant nonlinear selection gradient, negative static allometry, and a low degree of phenotypic variation. Hind leg length might be under stabilizing selection in males if having average-sized legs facilitates female mounting or improves a male’s ability to achieve the appropriate copulation position. As predicted, a negative allometric scaling pattern and low phenotypic variation of clasper size is suggestive of stabilizing selection and supports the ‘one-size-fits-all’ hypothesis. Opposite to males, the mid and hind leg lengths of females showed positive static allometry. Relatively longer mid and hind leg lengths in larger females might benefit individuals via the better support of their larger abdomens. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, , ••‐••.

Relationships between masticatory rhythmicity, body mass and cephalometrically-determined aesthetic and functional variables during development in humans

ObjectiveWe studied the relationship between chewing rhythmicity, craniomandibular morphology, and age in humans. DesignSixty subjects (10M:10F/group×three age groups, viz., 4–8, 10–14, and 17–21 years) participated. Subjects chewed gum for 2min while jaw movements in the frontal plane were videorecorded. Mean and variation in mean chewing cycle duration (TC) were quantified using maximum opening to maximum opening as cycle boundaries. Five “aesthetic” cephalometric variables (e.g., ANB) and seven “functional” variables (e.g., jaw length) were quantified from subjects’ lateral cephalographs. Simple linear regression models and several multivariate analyses were used in comparisons. ResultsMean TC increased and variation in TC decreased significantly with age. Body mass correlated with age, height, TC, all seven “functional” variables and only two “aesthetic” variables. Mean TC was correlated significantly with jaw length, distance from condylion to first molar point, distance from gonion to zygomatic arch, and distance from hyoid to menton. ConclusionsTC appeared to adapt with age. Although TC scaled most significantly with age, it is more likely that TC is mechanistically linked to jaw length or size. The decrease in TC variation with age suggests improved efficiency. TC did not scale with “aesthetic” variables, suggesting that these do not impact chewing rate; however, clinical procedures that impact jaw length may. The negative allometric scaling of TC with “functional” variables may reflect the pedomorphic jaw and face of humans. Further human studies will provide insights into the nature of scaling and adaptation of rhythmic chewing during development.

Twig size-number trade-off among woody plants in Tiantong region, Zhejiang Province of China

Aims The branch size-number trade-off among woody plants has implications for both the formation of plant architecture and biomass allocation in response to environment stresses.Our objective was to examine how the twig size-number relationship varies among woody plants in subtropical broad-leaved evergreen forests in south-eastern China.Methods The study site is located in Tiantong National Forest Park(29°52' N,121°39' E),Zhejiang Province,in Eastern China.We measured twig length,twig diameter,number of twigs and length and diameter of branches from which the twigs were sampled for 76 woody species in a 1-hm-2 plot.Standardized major axis(SMA) analysis was conducted to examine the quantitative relationship between twig size(cross-sectional area) and the number of twigs at a given twig size(twig intensity).Important findings A significantly negative allometric scaling relationship was found between twig intensity and its cross-sectional area.Under level-Ⅱ light exposure(LE-Ⅱ,40%-80% of the plant under direct light),ever-green species had a much higher twig intensity than deciduous species.However,there was no difference in twig intensity between these two life forms under LE-Ⅰ(40% ehxposure) or LE-Ⅲ(80% exposure).Higher twig intensity was found in evergreen species under LI-Ⅲ than under both LE-Ⅰ and LE-Ⅱ.In contrast,twig intensity of deciduous species was not different among any of the light exposure levels.Shrubs 4 m height had higher twig intensity than sub-trees and trees 4 m at a given twig size.We conclude that the twig size-number trade-off across woody plants in Tiantong was consistent with the Corner's rule(that describes the relationship between twig size and the number of twigs),but might differ among different life forms.Both evergreen species and shrubs are inclined to develop higher twig intensity,which indicates their adaptation to environment stress caused by limitations in light availability.

Negative allometry of docosahexaenoic acid in the fowl lung and pulmonary surfactant phospholipids

In a recent study (Comp. Biochem. Physiol. B. (2010)155: 301-308) we reported that the fatty acids (FA) of the avian (7 species) total lung phospholipids (PL) (i.e. lung parenchyma and surfactant together) provide allometric properties. To test whether this allometric scaling also occurs in either of the above components, in six gallinaceous species, in a body weight range from 150 g (Japanese quail, Coturnix coturnix japonica) to 19 kg (turkey, Meleagris gallopavo) the PL FA composition (mol%) was determined in the pulmonary surfactant, in native and in thoroughly lavaged lungs (referred to as lung parenchyma). In all three components docosahexaenoic acid (DHA) showed significant and negative allometric scaling (B = -0.056, -0.17 and -0.1, respectively). Surfactant PLs provided further negative allometry for palmitic acid and the opposite was found for palmitoleate and arachidonate. In the lung parenchymal PLs increasing body weight was matched with shorter chain FAs (average FA chain length) and competing n6 and n3 end-product fatty acids (positive allometry for arachidonic acid and negative for DHA). Negative allometric scaling was found for the tissue malondialdehyde concentration in the native and lavaged lungs (B = -0.1582 and -0.1594, respectively). In these tissues strong correlation was found between the MDA concentration and DHA proportion (r = 0.439 and 0.679, respectively), denoting the role of DHA in shaping the allometric properties and influencing the extent of in vivo lipid peroxidation of membrane lipids in fowl lungs.

Metabolic rate and food availability of the Antarctic amphipod Gondogeneia antarctica (Chevreux 1906): seasonal variation in allometric scaling and temperature dependence

Among the few existing works on seasonal variation in metabolic rate of polar species, most have been conducted during summer due to logistic constraints and have been focused on species that cease feeding during winter. In this work, we present the first extensive data set on the seasonal variation in metabolic rate of G. antarctica, an abundant amphipod that feeds throughout the year, and its relationship with body size, potential food availability and temperature. We measured the resting metabolic rate (RMR) of groups of individuals during 6 months from late summer through winter at 4 experimental temperatures and for a wide range of body size. RMR had a negative allometric scaling with body size and showed a tendency to increase with temperature as expected. However, temperature and body size effects on RMR showed a significant temporal variation, and an increase in temperature decreased scaling exponents. RMR at the mean seawater temperature throughout the study showed a strong seasonal variation following food availability: RMR decreased from the end of summer through winter, coinciding with a reduction in microphytobenthos stock, but recovered summer values in August, when an epontic algae boom occurred. The seasonal factorial aerobic scope (×2.37) is lower than benthic Antarctic invertebrates that cease feeding during winter, in agreement with what is expected based on theoretical grounds. Results suggest that seasonal variation of RMR would allow G. antarctica to achieve a high efficiency in energy utilization, while maintaining the ability to exploit sudden changes in food supply.

Allometric Scaling of Metabolism, Growth, and Activity in Whole Colonies of the Seed‐Harvester AntPogonomyrmex californicus

The negative allometric scaling of metabolic rate with body size is among the most striking patterns in biology. We investigated whether this pattern extends to physically independent eusocial systems by measuring the metabolic rates of whole functioning colonies of the seed-harvester ant Pogonomyrmex californicus. These intraspecific scaling data were compared to the predictions of an additive model developed to estimate collective metabolic rates. Contrary to the prediction of the additive model, colony metabolic rate allometry resembled the pattern commonly observed interspecifically for individual organisms, scaling with colony mass(0.75). Among the same-aged colonies, net growth rate varied by up to sevenfold, with larger colonies exhibiting higher net growth efficiency than smaller colonies. Isolated worker groups exhibited isometric metabolic rate scaling, suggesting that the social environment of the colony is critical to regulating individual patterns of work output. Within the social environment, individual worker locomotor velocities exhibited power-law distributions that scaled with colony size so that larger colonies exhibited a greater disparity between active and inactive ants than did smaller colonies. These results demonstrate that behavioral organization within colonies may have a major influence on colony-level metabolism and in generating intraspecific variation in growth trajectories.

Fast and furious: effects of body size on strike performance in an arboreal viperTrimeresurus(Cryptelytrops)albolabris

Body size has a pervasive effect on animal functioning and life history with size dependent changes in performance and physiology throughout ontogeny being common in many ectothermic vertebrates. However, as selection on juvenile life history stages is strong, juveniles often offset the disadvantages of small body size by disproportionate levels of performance. Here, we investigate size-related changes in defensive strike performance in an arboreal pit viper, Trimerusurus (Cryptelytrops) albolabris. Our data show a significant negative allometry in the scaling of head dimensions and head mass to body mass. However, strike velocity and strike distance are independent of body mass, with juveniles in our sample striking as fast and as far as adults. In contrast to model predictions suggesting that acceleration capacity should decrease with increasing body mass, acceleration capacity increases with snake body mass. Our results suggest that this is the result of a negative allometric scaling of head mass combined with an isometric scaling of the dorsal epaxial musculature. Finally, our data show a significant sexual dimorphism in body size and strike velocity with females being heavier and striking faster independent of the dimorphism in body size.

Allometric scaling of fatty acyl chains in fowl liver, lung and kidney, but not in brain phospholipids

The phospholipid (PL) fatty acyl chain (FA) composition (mol%) was determined in the kidney, liver, lung and brain of 8 avian species ranging in body mass from 150g (Japanese quail, Coturnix coturnix japonica) to 19kg (turkey, Meleagris gallopavo). In all organs except the brain, docosahexaenoic acid (C22:6 n3, DHA) was found to show a negative allometric scaling (allometric exponent: B=-0.18; -0.20 and -0.24, for kidney, liver and lung, respectively). With minor inter-organ differences, smaller birds had more n3 FAs and longer FA chains in the renal, hepatic and pulmonary PLs. Comparing our results with literature data on avian skeletal muscle, liver mitochondria and kidney microsomes and divergent mammalian tissues, the present findings in the kidney, liver and lung PLs seem to be a part of a general relationship termed "membranes as metabolic pacemakers". Marked negative allometric scaling was found furthermore for the tissue malondialdehyde concentrations in all organs except the brain (B=-0.17; -0.13 and -0.05, respectively). In the liver and kidney a strong correlation was found between the tissue MDA and DHA levels, expressing the role of DHA in shaping the allometric properties of membrane lipids.

Pitfalls in understanding the functional significance of genital allometry

The male genitalia of arthropods consistently show negative static allometry (the genitalia of small males of a species are disproportionally large, and those of large males are disproportionally small). We discuss relations between the 'one-size-fits-all' hypothesis to explain this allometry and the regimes of selection that may be acting on genitalia. We focus on the contrasts between directional vs. stabilizing selection, and natural vs. sexual selection. In addition, we point out some common methodological problems in studies of genital allometry. One-size-fits-all types of arguments for negative allometry imply net stabilizing selection, but the effects of stabilizing selection on allometry will be weaker when the correlation between body size and the trait size is weaker. One-size-fits-all arguments can involve natural as well as sexual selection, and negative allometry can also result from directional selection. Several practical problems make direct tests of whether directional or stabilizing selection is acting difficult. One common methodological problem in previous studies has been concentration on absolute rather than relative values of the allometric slopes of genitalia; there are many reasons to doubt the usefulness of comparing absolute slopes with the usual reference value of 1.00. Another problem has been the failure to recognize that size and shape are independent traits of genitalia; rapid divergence in the shape of genitalia is thus not paradoxical with respect to the reduced variation in their sizes that is commonly associated with negative allometric scaling.

A morphometric analysis of polymorphism in the pharyngeal dentition of Cichlasoma minckleyi (Teleostei: Cichlidae)

Dental polymorphism in teleost fishes often involves production of a robust dentition, or “molarization”, in one morph. The lower pharyngeals of a sample of wild-caught individuals of the polymorphic Cuatro Cienegas cichlid, Cichlasoma minckleyi (Kornfield and Taylor) (Proc. Biol. Soc. Wash. 96 (1983) 253), were measured to investigate morphological changes associated with molarization. Principal components analysis demonstrates that dental variability in this species increases in larger fish, and that only the molariform morph contributes to this increase. Reduced major axis regression analyses between pairs of variables indicate that the papilliform morph increases both tooth measures and numbers, whereas the molariform morph maintains a relatively constant number of teeth as it produces teeth of progressively larger size. In the papilliform morph, negative allometric scaling between tooth size and dentigerous area is compensated for by addition of teeth. Tooth size variables are isometric in the molariform morph, and tooth numbers are nearly static. These results are consistent with those reported for other polymorphic cichlid species. Further study is required to elucidate the mechanisms whereby tooth form in polyphyodont species may respond to environmental factors (like food hardness), but possibilities include direct mechanical influences or transmission of signals via nerves to developing replacement teeth.

Scaling of anaerobic metabolism during exercise in the estuarine crocodile (Crocodylus porosus)

The allometry of anaerobic metabolism was examined in wild estuarine crocodiles (Crocodylus porosus) exercised to exhaustion during capture, with the aim of identifying factors underlying the higher anaerobic capacity but possibly lower anaerobic scope in larger animals. Exercise time to exhaustion, and concentrations of lactate and protons in blood and tail muscle, increased with increasing body mass. Muscle glycogen, both before and after exercise, also showed positive allometric scaling. Muscle intracellular pH buffering capacity scaled negatively with body mass. The effects of pH on the activities of muscle phosphorylase and phosphofructokinase were independent of body mass. It is proposed that anaerobic capacity may be limited by the size of muscle glycogen reserves in smaller crocodiles and by glycolytic inhibition at the lower pH values encountered in larger crocodiles. Mean anaerobic scope, and phosphorylase activity in tail muscle, decreased with increasing body mass, while lactate dehydrogenase activity was independent of body mass. Negative allometric scaling of anaerobic scope in crocodiles may relate to changes in predator-prey and social interactions that involve reduced dependence on frequent bursts of anaerobic muscle work with increasing body mass.