Temperature-mediated transitions between isometry and allometry in a colonial, modular invertebrate

The evolutionary success of animal design is strongly affected by scaling and virtually all metazoans are constrained by allometry. One body plan that appears to relax these constraints is a colonial modular (CM) design, in which modular iteration is hypothesized to support isometry and indeterminate colony size. In this study, growth rates of juvenile scleractinians (less than 40mm diameter) with a CM design were used to test this assertion using colony diameters recorded annually for a decade and scaling exponents (b) for growth calculated from double logarithmic plots of final versus initial diameters. For all juvenile corals, b differed significantly among years, with isometry (b=1) in 4 years, but positive allometry (b>1) in 5 years. The study years were characterized by differences in seawater temperature that were associated significantly with b for growth, with isometry in warm years but positive allometry in cool years. These results illustrate variable growth scaling in a CM taxon and suggest that the switch between scaling modes is mediated by temperature. For the corals studied, growth was not constrained by size, but this outcome was achieved through both isometry and positive allometry. Under cooler conditions, positive allometry may be beneficial as it represents a growth advantage that increases with size.     

Allometry and adaptation in the catarrhine postcranial skeleton

Seven measurements were taken on the postcranial skeleton of 249 specimens representing ten species of catarrhine primates and tested to determine their relationship with size. Size was measured as skeletal weight on each individual. It was found that the interspecific line based on the entire sample was in some cases determined not only by morphological adjustments for size variation but also by changes in locomotor adaptations of differently sized species within the sample. It is suggested that it is consequently preferable to study allometric relationships within a species or within a group of species that differ in size but are similar in their mode of locomotion. The allometric analysis reveals some interesting patterns within the data. Limb lengths scaled with either negative allometry or isometry over the entire sample. Within the species groups isometry was the rule except for pongid femurs, which showed negative scaling. Humerus length scaled at the same rate in pongids as in cercopithecoids but had a slightly higher intercept value. While colobines and cercopithecines scaled at similar rates for all seven dimensions, the colobine line was shifted to a position above that for cercopithecines in every case. It is suggested that this is a result of adaptation for leaping in the former group. Other implications of the allometric results are discussed.     

Determinate growth and the scaling of photosynthetic energy intake in the solitary coral Fungia concinna (Verrill)

For many marine invertebrates, the maximum size of an individual is influenced heavily by environmental factors and may be limited by energetic constraints. In this study, an energetic model developed originally for anemones was applied to the free-living scleractinian Fungia concinna (Verrill) from Moorea (French Polynesia) to test the hypothesis that energetic constraints limit the size of this solitary coral. The modified model assumed that photosynthesis was the primary source of metabolic energy, and that metabolic costs were represented by aerobic respiration; these sources and sinks of energy were compared using daily energy budgets that were analyzed using double logarithmic regressions of energy against coral size. With this approach, energy limitation is characterized by a scaling exponent for energetic cost (b_cost) that is larger than the scaling exponent for energy intake (b_intake). For the size range of F. concinna studied, b_intake = 0.73 ± 0.09 and b_cost = 0.46 ± 0.10, thereby demonstrating that large individuals accumulated an energetic surplus, even when the expenditure associated with host tissue and symbiont growth was included in the model. The surplus of energy that this coral acquires as it grows appears to be driven by the scaling of traits associated functionally with the scaling of respiration and photosynthesis. Specifically, tissue biomass displayed a strong positive allometry with respect to surface area (i.e., b > 1), and this constraint on surface area may be the mechanistic basis of the low scaling exponent for metabolic cost. In contrast, the capacity for autotrophy - defined indirectly as Symbiodinium population density and chlorophyll content - increased isometrically with surface area, and likely contributed to the higher scaling exponent for intake relative to cost. Our results suggest that growth in F. concinna is not limited strictly by energy, but instead maximum size must be determined by alternative physiological or ecological constraints.     

Do insect metabolic rates at rest and during flight scale with body mass?

Energetically costly behaviours, such as flight, push physiological systems to their limits requiring metabolic rates (MR) that are highly elevated above the resting MR (RMR). Both RMR and MR during exercise (e.g. flight or running) in birds and mammals scale allometrically, although there is little consensus about the underlying mechanisms or the scaling relationships themselves. Even less is known about the allometric scaling of RMR and MR during exercise in insects. We analysed data on the resting and flight MR (FMR) of over 50 insect species that fly to determine whether RMR and FMR scale allometrically. RMR scaled with body mass to the power of 0.66 (M0.66), whereas FMR scaled with M1.10. Further analysis suggested that FMR scaled with two separate relationships; insects weighing less than 10mg had fourfold lower FMR than predicted from the scaling of FMR in insects weighing more than 10mg, although both groups scaled with M0.86. The scaling exponents of RMR and FMR in insects were not significantly different from those of birds and mammals, suggesting that they might be determined by similar factors. We argue that low FMR in small insects suggests these insects may be making considerable energy savings during flight, which could be extremely important for the physiology and evolution of insect flight.     

Scaling of follicular sizes in mammalian ovaries

The scaling of ovarian follicle and oocyte sizes according to body weight ( M , ranging from 0005–500 kg) has been analysed using data obtained from 22 mammalian species in nine orders. The diameters of non-growing (primordial) follicles were correlated significantly with body weight, the relationship being described by the allometric formula y = 0028 M ^0.10. The mean size at which growing follicles began to accumulate extracellular fluid was approximately the same in all species, 0–3 mm diameter. Graafian follicle sizes varied allometrically with body weight as a result of differences in the volumes of follicular fluid rather than those of oocytes, which were relatively similar in eutherian mammals. The statistical significance of the correlation between Graafian and body sizes was increased when the dimensions for an ovulatory quota of follicles were combined because follicles in polyovulating species were disproportionately small. The total Graafian surface areas and volumes were then predicted from body weight by 58–4 M ^0.65 and 18–5 M ^1.06, respectively. Follicular dimensions in the three species of primates were significantly greater than predicted by the allometric relationship. The exponents of these relationships show that the total volume of a set of preovulatory follicles varies approximately isometrically with body weight and, therefore, with the presumptive hormone distribution volume ( M ^1.0). The hypoallometric relationship of follicular surface area demonstrates that, during the course of the evolution of body size, the surface area for secretion has not increased to match the dilution of hormones in the body pool.     

The effect of flow and morphology on boundary layers in the scleractinians Dichocoenia stokesii (Milne-Edwards and Haime) and Stephanocoenia michilini (Milne-Edwards and Haime)

Mass transfer characteristics of scleractinian corals are affected by their skeletal morphology and the concentration gradients that develop as a consequence of the interactions of their morphology and biomass with the overlying seawater. These interactions can have a profound effect on coral metabolism. In this study, boundary layer characteristics were compared between different size colonies of the corals Dichocoenia stokesii and Stephanocoenia michilini to determine the relative roles of colony size and corallite structures (i.e. surface roughness) in mass transfer. Colonies of both species were rounded in shape, but differed in small-scale roughness as measured by the elevation of corallites. Additionally, D. stokesii had a greater aspect ratio than S. michilini, and their colonies were slightly taller for a given diameter. Boundary layers were characterized by placing dead coral skeletons in a flow tank and estimating shear velocities (u(*)) at different flow speeds. The effects of flow speed, size, and roughness on shear velocities were estimated for two juvenile size classes (10-20 and 30-40 mm diameter) of each species that were exposed to unidirectional flow regimes (4 and 17 cm s(-1)). Shear velocities were significantly greater in high, compared to low flow, and there was a significant interaction between colony size and surface roughness; the interaction was caused by a difference in magnitude, rather than direction, of the effect of roughness and size on u(*). Thus, there was a greater degree of turbulence at high flow compared to low flow, regardless of roughness or size, and the greatest turbulence occurred over large colonies of D. stokesii at high flow. Together, these results suggest that boundary layers around small corals are heavily influenced by upstream roughness elements, and more strongly affected by flow regimes than skeletal features. The relationship between colony morphology (i.e. aspect ratio and, possibly, surface roughness) and boundary layer characteristics may be non-linear in small corals.     

Excavation and architecture of Argentine ant nests

We used x-ray computed tomography to study the elaboration of nest structures in small sand-filled nest boxes by Argentine ant (Linepithema humile) colonies composed of 10, 100, and 1000 workers. The pattern of nest growth was consistent with a process of density-dependent stimulation of excavation, which subsided as nests grew and the density of digging stimuli declined. Thus, nest excavation would be auto-regulating, and final nest size should be adjusted to colony size. We found that excavation rates and final nest sizes increased with colony size, but were not tenfold greater in 1000-worker colonies than in 100-worker colonies. In the largest colonies, the internal surface area scaled allometrically with volume, so that more surface was obtained relative to volume excavated as the nest grew. Although the gross features of Argentine ant nests, such as total size, seem explicable by a simple, self-organized regulatory process, other features of the nest architecture will require further investigation. Received 3 March 2005; revised 26 April 2005; accepted 3 May 2005.     

On the allometry of biomass partitioning and light harvesting for plants with leafless stems

Prior explicit allometric models are extended to predict the scaling relationship between the ability of plants with leafless stems to harvest sunlight H and total standing plant biomass M(T) (which equals the sum of standing stem and root biomass, M(S) and M(R)). Provided that H scales in a directly proportional manner (isometrically) with respect to either stem surface area (i.e.H proportional, variant SA(S) ) or total stem biomass (i.e. H proportional, variant M(S)), the allometric model presented here predicts that SA(S) proportional, variant M(T)(3/4) or M(S) proportional, variant M(T)(3/4), respectively. These alternative predictions are tested empirically using data for standing stem and root biomass gathered for the large columnar cactus species Pachycereus pringlei. Statistical comparisons between observed and predicted scaling relationships indicate that SA(S) proportional, variant M(T)(3/4), whereas M(S) proportional, variant M(T)(3/4) is mathematically inconsistent with the observation that stem biomass scales nearly isometrically with respect to root biomass. The contention that the H of leafless stems scales isometrically with respect to stem surface area is thus reasonable both theoretically and empirically.     

Influence of food,body size,and fragmentation on metabolic rate in a sessile marine invertebrate

Metabolic rates vary among individuals according to food availability and phenotype, most notably body size. Disentangling size from other factors (e.g., age, reproductive status) can be difficult in some groups, but modular organisms may provide an opportunity for manipulating size experimentally. While modular organisms are increasingly used to understand metabolic scaling, the potential of feeding to alter metabolic scaling has not been explored in this group. Here, we perform a series of experiments to examine the drivers of metabolic rate in a modular marine invertebrate, the bryozoan Bugula neritina. We manipulated size and examined metabolic rate in either fed or starved individuals to test for interactions between size manipulation and food availability. Field collected colonies of unknown age showed isometric metabolic scaling, but those colonies in which size was manipulated showed allometric scaling. To further disentangle age effects from size effects, we measured metabolic rate of individuals of known age and again found allometric scaling. Metabolic rate strongly depended on access to food: starvation decreased metabolic rate by 20% and feeding increased metabolic rate by 43%. In comparison to other marine invertebrates, however, the increase in metabolic rate, as well as the duration of the increase (known as specific dynamic action, SDA), were both low. Importantly, neither starvation nor feeding altered the metabolic scaling of our colonies. Overall, we found that field‐collected individuals showed isometric metabolic scaling, whereas metabolic rate of size‐manipulated colonies scaled allometrically with body size. Thus, metabolic scaling is affected by size manipulation but not feeding in this colonial marine invertebrate.     

Colony versus population variation in susceptibility and resistance to dark spot syndrome in the Caribbean coral Siderastrea siderea

Scleractinian corals appear to be increasingly susceptible to pathogenic diseases, yet it is poorly understood why certain individuals, populations or species are more susceptible to diseases than others. Clearly an understanding of mechanisms of disease resistance in corals is essential to our understanding of patterns of disease incidence and virulence; this work must begin by examining the colony and population levels of organization. The Caribbean coral Siderastrea siderea exhibits variability in susceptibility to dark spot syndrome (DSS), a disease of unknown origin that can result in tissue necrosis. On the reef scale, variability in DSS prevalence in S. siderea occurred through time, but was not correlated with site, seawater temperature or depth. We monitored colonies of S. siderea affected by DSS, as well as their nearest neighbor controls, for 2 years in the Bahamas and found a marked decline in extent of DSS infection in October of both years. A preliminary survey of antimicrobial activity in S. siderea indicated selective activity against certain ecologically relevant bacteria. To assess whether changes in chemical defenses were responsible for the observed temporal variability in DSS prevalence, we sampled S. siderea for qualitative and quantitative analysis of chemical variability between resistant and susceptible colonies of S. siderea. These data suggest that phenotypic plasticity in antimicrobial activity may impact microbial settlement and/or survival.     

Allometry in the giant tropical ant, Paraponera clavata

Summary: Workers of the ponerine ant, Paraponera clavata, grow allometrically, with the head disproportionately larger in larger workers. The anterior (clypeus)-posterior (occiput) dimension of the head capsule is allometric with the lateral (interocular) dimension, so that larger workers have elongate heads. The degree of head capsule allometry varies among colonies; this could result either from differences in colony maturity or from variation in developmental patterns among colonies. These data resolve a previously controversial issue concerning caste in Paraponera clavata.     

Morphological Diversity Despite Isometric Scaling of Lever Arms

In the absence of a substantial functional shift, morphological evolution is usually expected to follow an allometric trajectory, however, studies of tree squirrel jaws have found isometry across most of their size range. This isometry appears to reflect the integration of a small number of lever arm lengths that are critical for generating bite force. To test whether this integration constrains only the ratios of these lengths, or jaw shape in general, we analyzed jaw shapes and a set of lengths comparable to those used in previous studies for 23 species of sciurine tree squirrels (Sciurus, Tamiasciurus and Microsciurus), a lineage that is both functionally uniform and spans a large size range. We found that the measured lengths were highly correlated and isometric with respect to each other, but negatively allometric with respect to jaw size. Shape differences are generally small, but shape diversity was still greater than the diversity of mechanical advantages (input lever lengths scaled by output lever length). In addition, phylogenetic analyses demonstrated that only a minute fraction of shape evolution is correlated with size evolution. This contrast between the diversity of shape and the stability of proportions among a suite of functionally relevant lengths suggests that constraints on those lengths and the associated mechanical parameters have little or no ability to restrict changes in other aspects of jaw form.     

Consequences of fission in the coral <Emphasis Type="Italic">Siderastrea siderea</Emphasis>: growth rates of small colonies and clonal input to population structure

Colony age and size can be poorly related in scleractinian corals if colonies undergo fission to form smaller independent patches of living tissue (i.e., ramets), but the implications of this life-history characteristic are unclear. This study explored the ecological consequences of the potential discrepancy between size and age for a massive scleractinian, first by testing the effect of colony origin on the growth of small colonies, and second by quantifying the contribution of ramets to population structure. Using Siderastrea siderea in St. John (US Virgin Islands) as an experimental system, the analyses demonstrated that the growth of small colonies derived from sexual reproduction was 2.5-fold greater than that of small ramets which were estimated to be ≈100 years older based on the age of the parent colonies from which they split. Although fission can generate discrete colonies, which in the case of the study reef accounted for 42% of all colonies, it may depress colony success and reef accretion through lowered colony growth rates.     

Fungi in Porites lutea: association with healthy and diseased corals.

Healthy and diseased scleractinian corals have been reported to harbour fungi. However, the species of fungi occurring in them and their prevalence in terms of biomass have not been determined and their role in coral diseases is not clear. We have found fungi to occur regularly in healthy, partially dead, bleached and pink-line syndrome (PLS)-affected scleractinian coral, Porites lutea, in the reefs of Lakshadweep Islands in the Arabian Sea. Mostly terrestrial species of fungi were isolated in culture from these corals. Hyaline and dark, non-sporulating fungi were the most dominant forms. Fungal hyphae extended up to 3 cm within the corals. Immunofluorescence detection using polyclonal immunological probes for a dark, initially non-sporulating isolate (isolate # 98-N28) and for a hyaline, non-sporulating fungus (isolate # 98-N18) revealed high frequencies of these in PLS-affected, dead and healthy colonies of P. lutea. Total fungal biomass accounted for 0.04 to 0.05% of the weight of corals in bleached corals and was higher than in PLS-affected and healthy colonies. Scanning electron microscopy revealed the presence of fungi within the carbonate skeleton and around polyps. Fungi appear to be a regular component of healthy, partially dead and diseased coral skeleton.     

The combined effect of body size and temperature on oxygen consumption rates and the size-dependency of preferred temperature in European perch Perca fluviatilis

The present study determined the effect of body mass and acclimation temperature (15–28°C) on oxygen consumption rate (ṀO₂) and the size dependency of preferred temperature in European perch Perca fluviatilis. Standard metabolic rate (SMR) scaled allometrically with body mass by an exponent of 0.86, and temperature influenced SMR with a Q₁₀ of 1.9 regardless of size. Maximum metabolic rate (MMR) and aerobic scope (MMR-SMR) scaled allometrically with body mass by exponents of 0.75–0.88. The mass scaling exponents of MMR and aerobic scope changed with temperature and were lowest at the highest temperature. Consequently, the optimal temperature for aerobic scope decreased with increasing body mass. Notably, fish <40 g did not show a decrease aerobic scope with increasing temperature. Factorial aerobic scope (MMR × SMR⁻¹) generally decreased with increasing temperatures, was unaffected by size at the lower temperatures, and scaled negatively with body mass at the highest temperature. Similar to the optimal temperature for aerobic scope, preferred temperature declined with increasing body mass, unaffectedly by acclimation temperature. The present study indicates a limitation in the capacity for oxygen uptake in larger fish at high temperatures. A constraint in oxygen uptake at high temperature may restrict the growth of larger fish with environmental warming, at least if food availability is not limited. Furthermore, behavioural thermoregulation may be contributing to regional changes in the size distribution of fish in the wild caused by global warming as larger individuals will prefer colder water at higher latitudes and at larger depths than smaller conspecifics with increasing environmental temperatures.     

Evolutionary ecology of colonial reef-organisms, with particular reference to corals

Sedentary reef-organisms such as sponges, colonial coelenterates, bryozoans and compound ascidians produce repeated modules (aquiferous systems, polyps, zooids) as they grow. Modular construction alleviates constraints on biomass imposed by mechanical and energetic factors that are functions of the surface area to volume ratio. Colonies thus may grow large whilst preserving optimal modular dimensions. Among corals, optimal polyp size is smaller in the more autotrophic than in the more heterotrophic species. Modular construction allows flexibility of growth form, which can adapt to factors such as water currents, silting, light intensity and proximity of competitors. Modular colonies have great regenerative capacities, even separated fragments may survive and grow into new colonies. All fragments from a parental colony are genetically identical and large branching corals frequently undergo clonal propagation through fragmentation during storms. Soft corals can also fragment endogenously. By spreading the risk of mortality among independent units, the generation and dispersal of fragments lessens the likelihood of clonal extinction. In spite of their ability to propagate asexually, most benthic colonial animals also reproduce asexually. The selective advantages of the genetic diversity among sexually produced offspring seem not to be linked with dispersal, but probably lie in the biological interactions with competitors, predators and pathogens in the parental habitat. Age at first sexual maturity and the proportional investment of resources in sexual reproduction are related to colonial survivorship. Small branching corals on reef flats grow quickly, attain sexual maturity within 1–4 years, planulate extensively, but reach only small sizes before dying. Massive corals are longer lived and have the opposite characteristics of growth and reproduction. Most sessile reef organisms compete for space, food or light. Faster growers can potentially outcompete slower growers, but are often prevented from doing so by several forms of aggression from competitors and by the damage inflicted by storms. Competitive interactions among sedentary organisms on coral reefs are unlikely to be linear or deterministic, and so the co-existence of diverse species is possible.     

Scaling of postcontractile phosphocreatine recovery in fish white muscle: effect of intracellular diffusion

In some fish, hypertrophic growth of white muscle leads to very large fibers. The associated low-fiber surface area-to-volume ratio (SA/V) and potentially long intracellular diffusion distances may influence the rate of aerobic processes. We examined the effect of intracellular metabolite diffusion on mass-specific scaling of aerobic capacity and an aerobic process, phosphocreatine (PCr) recovery, in isolated white muscle from black sea bass (Centropristis striata). Muscle fiber diameter increased during growth and was >250 mum in adult fish. Mitochondrial volume density and cytochrome-c oxidase activity had similar small scaling exponents with increasing body mass (-0.06 and -0.10, respectively). However, the mitochondria were more clustered at the sarcolemmal membrane in large fibers, which may offset the low SA/V, but leads to greater intracellular diffusion distances between mitochondrial clusters and ATPases. Despite large differences in intracellular diffusion distances, the postcontractile rate of PCr recovery was largely size independent, with a small scaling exponent for the maximal rate (-0.07) similar to that found for the indicators of aerobic capacity. Consistent with this finding, a mathematical reaction-diffusion analysis indicated that the resynthesis of PCr (and other metabolites) was too slow to be substantially limited by diffusion. These results suggest that the recovery rate in these fibers is primarily limited by low mitochondrial density. Additionally, the change in mitochondrial distribution with increasing fiber size suggests that low SA/V and limited O(2) flux are more influential design constraints in fish white muscle, and perhaps other fast-twitch vertebrate muscles, than is intracellular metabolite diffusive flux.     

Energetic inequivalence in eusocial insect colonies

The energetic equivalence rule states that population-level metabolic rate is independent of average body size. This rule has been both supported and refuted by allometric studies of abundance and individual metabolic rate, but no study, to my knowledge, has tested the rule with direct measurements of whole-population metabolic rate. Here, I find a positive scaling of whole-colony metabolic rate with body size for eusocial insects. Individual metabolic rates in these colonies scaled with body size more steeply than expected from laboratory studies on insects, while population size was independent of body size. Using consumer-resource models, I suggest that the colony-level metabolic rate scaling observed here may arise from a change in the scaling of individual metabolic rate resulting from a change in the body size dependence of mortality rates.     

A novel method for the transport and analysis of genetic material from polyps and zooxanthellae of scleractinian corals

We have developed a new simple method for transport, storage, and analysis of genetic material from the corals Agaricia agaricites, Dendrogyra cylindrica, Eusmilia ancora, Meandrina meandrites, Montastrea annularis, Porites astreoides, Porites furcata, Porites porites, and Siderastrea siderea at room temperature. All species yielded sufficient DNA from a single FTA card (19 microg-43 ng) for subsequent PCR amplification of both coral and zooxanthellar DNA. The D1 and D2 variable region of the large subunit rRNA gene (LSUrDNA) was amplified from the DNA of P. furcata and S. siderea by PCR. Electrophoresis yielded two major DNA bands: an 800-base pair (bp) DNA, which represented the coral ribosomal RNA (rRNA) gene, and a 600-bp DNA, which represented the zooxanthellar srRNA gene. Extraction of DNA from the bands yielded between 290 microg total DNA (S. siderea coral DNA) and 9 microg total DNA (P. furcata zooxanthellar DNA). The ability to transport and store genetic material from scleractinian corals without resort to laboratory facilities in the field allows for the molecular study of a far wider range and variety of coral sites than have been studied to date.     

亚热带常绿林不同冠层小枝叶面积-叶生物量关系研究

叶面积与叶生物量的关系对于理解植物叶片的碳收益和投资权衡策略具有重要意义。收益递减假说认为植物的叶面积与叶生物量成显著异速生长关系，其异速生长指数<1.0，但该假说是否适用于不同生活型（常绿与落叶）亚热带木本植物不同冠层高度（上下冠层）当年生小枝的叶片仍不清楚。以江西亚热带常绿阔叶林的69种常绿与落叶木本植物当年生小枝上的叶为研究对象，采用标准化主轴回归估计（standardized major axis estimation，SMA）方法检验不同冠层高度和生活型叶面积与叶生物量的异速生长关系。结果显示：（1）当年生小枝叶生物量在不同冠层高度和生活型的植物中无显著差异（P>0.05），叶面积在常绿和落叶植物中有显著差异（P<0.05），常绿和落叶植物的比叶重存在显著差异（P<0.05），而落叶植物的比叶重在不同冠层高度存在显著差异（P<0.05），同一冠层，常绿植物比叶重显著高于落叶植物（P<0.05）；（2）69种植物的叶面积与叶生物量异速生长指数具有物种特异性，60.9%的物种叶面积与叶生物量呈等速生长关系；（3）不同冠层和生活型植物的叶面积与叶生物量呈等速生长关系，但其异速生长常数在不同冠层高度与生活型间存在差异。这些结果表明冠层高度和生活型未改变叶面积-生物量之间的等速生长关系，不支持"收益递减"假说。