Metabolic level and size scaling of rates of respiration and growth in unicellular organisms

1.  Metabolic rate is conventionally assumed to scale with body mass to the 3/4-power, independently of the metabolic level of the organisms being considered. However, recent analyses in a variety of animals and plants indicate that the power (log–log slope) of this relationship varies significantly with metabolic level, ranging from c . 2/3 to 1.
2.  Here I show that the scaling slopes of rates of respiration and growth are related to the metabolic level of a variety of unicellular organisms, as similarly occurs for respiration rates in multicellular organisms.
3.  The recently proposed 'metabolic-level boundaries hypothesis' provides insight into these effects of metabolic level. As predicted, the scaling slopes for resting (endogenous) respiration rate in prokaryotes, algae and protozoans are negatively related to metabolic level; and in protozoans, the scaling slope increases with starvation. Also as predicted, the scaling slopes of growth rate in algae and protozoans are negatively related to growth level. Unexpectedly, opposite effects of starvation on the metabolic scaling slopes of unicellular prokaryotes (compared to that of eukaryotes) may be a spurious result of respiration measurements that did not adequately consider the effects of rapid cell multiplication in prokaryotes with extremely short generation times.
4.  Analyses of both unicellular and multicellular organisms show that there is no universal metabolic scaling relationship, and that variation in metabolic scaling relationships is systematically and possibly universally related to metabolic level.     

The size–grain hypothesis: do macroarthropods see a fractal world?

Abstract.  1. In the size–grain hypothesis (a) long legs allow walking organisms to step over gaps and pores in substrate but prohibit them from entering those gaps; (b) the world is more rugose for small organisms; and (c) the relative cost of long legs increases as organisms grow smaller. The hypothesis predicts a positive allometry of leg length ( = mass ^b where b > 0.33 of isometry), a pattern that robustly holds for ants.
2. Toward testing for leg length allometries in other taxa, arthropods were extracted from the Panama leaf litter and measured. Three common taxa (spiders, diplopods, Coleoptera) yielded b s that exceeded 0.33 while three others (Acarina, Pseudoscorpiones, and Collembola) did not. The exponent b tended to increase ( P = 0.06, n = 7) with an arthropod taxon's average body mass.
3. Since leg length in cursorial organisms tends toward isometry in very small and very large taxa (i.e. mammals) this suggests that the size–grain hypothesis may best apply at a transition zone of intermediate body mass: the macroarthropods.
4. Body length was a robust predictor of mass in all groups despite variation in shape.     

Population energy use scales positively with body size in natural aquatic microcosms

Aim  We test the 'energetic equivalence rule' (EER) – the idea that the amount of energy used by a population per unit area per unit time is independent of body mass – in meio-invertebrate communities from a series of natural, multitrophic aquatic 'rock pool' microcosms. Our study represents the first rigorous test of the EER at local scales of observation in a community of naturally coexisting species.
Location  Discovery Bay, Jamaica.
Method  We estimated population energy use (PEU) for every occurrence of every species of meio-invertebrate fauna found in each of 29 microcosms (233 observations of 31 species) using estimates of population density obtained in January 2005 in combination with published metabolism–mass relations for closely related taxa.
Results  In the rock pool system as a whole, population density decreased ( ancova : b  = –0.38 (–0.55 to –0.19), r ² = 0.19, P  < 0.001) and PEU increased with body mass ( ancova : b  = 0.55 (0.36–0.73), r ² = 0.28, P  < 0.001).
Main conclusions  The positive PEU–body mass relation found here suggests that larger organisms are energetically dominant and points to the importance of size-structured competition in these systems. Our results contrast those obtained in the few other previously published tests of the EER and challenge the idea that all species use similar amounts of energy regardless of their size.     

Effects of temperature, body size and feeding on rates of metabolism in young‐of‐the‐year haddock

The mean rate of oxygen consumption (routine respiration rate, R _R, mg O₂ fish⁻¹ h⁻¹), measured for individual or small groups of haddock Melanogrammus aeglefinus (3–12 cm standard length, L _S) maintained for 5 days within flow‐through respiratory chambers at four different temperatures, increased with increasing dry mass ( M _D). The relationship between R _R and M _D was allometric ( R _R = α  M ^b ) with b values of 0·631, 0·606, 0·655 and 0·650 at 5·0, 8·0, 12·0 and 15·0° C, respectively. The effect of temperature ( T ) and M _D on mean R _R was described by     indicating a Q ₁₀ of 2·27 between 5 and 15° C. Juvenile haddock routine metabolic scope, calculated as the ratio of the mean of highest and lowest deciles of R _R measured in each chamber, significantly decreased with temperature such that the routine scope at 15° C was half that at 5° C. The cost of feeding ( R _SDA) was c . 3% of consumed food energy, a value half that found for larger gadoid juveniles and adults.     

Plasticity in metabolic allometry: the role of dietary stoichiometry

Metabolism involves multiple elements. While we know much about the allometry in metabolic response of organisms to energy (carbon, C) availability, little is known about how different-sized organisms respond to the relative availability of elements. I experimentally manipulated availability of phosphorus (P) relative to C, to test whether dietary C : P affects metabolism in four species of Daphnia , spanning an order of magnitude in body mass. Results indicated that the slope of the relationship between individual respiration and body mass was M ^0.83 under a balanced diet (C : P c. 150), and M ^0.67 under an imbalanced diet (C : P c. 800). Increased respiration under dietary imbalance was not due to increased ingestion. The change in the scaling exponent was due to the greater respiratory response of smaller species to altered diets. Diet-induced metabolic plasticity contributes to variation in metabolic allometry, at least at such small scales of body size.     

Growth and morphological development of sagittal otoliths of larval and early juvenile Trachurus japonicus

The daily periodicity of growth increment formation in sagittal otoliths of jack mackerel Trachurus japonicus was validated by marking otoliths with alizarin complexone (ALC). Analysis of otoliths of known‐age juveniles confirmed that the first increment formed on day 3 after hatching, and was associated with first feeding. A total of 198 specimens, ranging from 2·6 to 49·2 mm in body length (notochord length or standard length) and from 7 to 78 days in age, were collected in the East China Sea and Tosa Bay, and used to examine the association between otolith morphological development and ontogenetic development. The relationship between body length ( L ) and otolith radius ( R ) was significantly described by the linear function L  = 2·65 + 0·0425 R ( n  = 198, r ² = 0·99, P  < 0·001), indicating that somatic growth history can be reconstructed from otolith growth patterns. The otolith was primarily spherical in the preflexion larval stage, and became elongated with notochord flexion. The first secondary primordium formed at c . 25 days, during the middle postflexion stage, and was associated with metamorphosis. By c . 42 days the sagittal otolith was adult‐like in morphology, with the primary growth zone enclosed by the marginal growth zone, except in the anterior rostrum area. Thus age, growth and developmental stages were recorded in sagittal otoliths during the larval and early juvenile stages of jack mackerel.     

The effects of body mass and feeding on metabolic rate in small juvenile Atlantic cod

Apparent specific dynamic action (SDA) amplitude in young juvenile Atlantic cod Gadus morhua (1 to 8 g wet mass), fed a standardized meal and then exercised in a circular swimming respirometer at a constant swimming speed of 0·5 ± 0·3 body lengths s^-1, occurred within l h after feeding in all juveniles. SDA amplitude were 1·4 to 1·8 times higher in fed fish compared to unfed fish, and rates of oxygen consumption decreased as body mass increased. SDA duration had a tendency to decrease with increasing body mass and was shortest, at 6 h, in the smallest fish (1–1·5 g), but increased to 10–11 h in the largest fish. Apparent SDA in fed fish ( R _r) scaled with a mass exponent of 0·89, while maximum metabolic rate ( R _max) determined by chasing fish to exhaustion and then measuring oxygen consumption for 12 h, and unfed routine metabolic rate (R_r) scaled with a mass exponent of 0·79 and 0·76 respectively. Relative aerobic scope ( R _max– unfed R _r) did not appear to vary over the 1 to 8 g increase in wet mass. These results show that as body mass increased in young juvenile Atlantic cod: (1) apparent SDA ( R _f) increased more rapidly than R _max, and (2) apparent SDA took up >98% of the relative aerobic scope and that young Atlantic cod allocated most of the energy to growth, and left little for other metabolic activities.     

Larval Konosirus punctatus(Clupeidae) in a brackish river mouth on the Pacific coast of central Japan

Eggs of Konosirus punctatus in early developmental stages were collected from the eastern part of the mouth of Sagami Bay on the Pacific coast of central Japan. Advanced‐stage eggs and early larvae with notochord length ( L _N) of <7·5 mm were collected from the inner bay near the mouth of the Sagami River. Feeding larvae of >8·4 mm L _N were distributed in the mouth of the river, and juveniles of 24–90 mm standard length ( L _S) were collected from the lower reaches of the river between the river mouth and c . 3 km upstream of the river mouth. Hatch dates of larvae and juveniles collected in 2001 ( n  = 158) and in 2002 ( n  = 109) extended from late March to late July. The relationship between the otolith radius ( R _O) and L _N or L _S changed during the metamorphosis stage as characterized by 320 μm R _O and 22 mm L _S. Otolith growth rate, as an index of somatic growth rates in larval and early juvenile stages, was higher in cohorts that hatched later in the spawning season, i.e . from March to July. Konosirus punctatus that were spawned in the bay mouth area survived with different growth histories in the bay and lower reaches of the river, and recruited to the young‐of‐year population in the Pacific coastal waters of central Japan.     

Post-fledging body mass increase in Common Terns Sterna hirundo: influence of age, sex and year

We studied the inter-year and inter-sex variation of the post-fledging body mass development of Common Terns Sterna hirundo in 2000 and 2001 at the Banter See colony, northern Germany. Here, post-fledglings can be identified and weighed remotely and automatically by a transponder system that makes use of automated balances installed at the colony. Individuals were sexed with PCR amplification methods. After fledging, young generally continued to increase their mass. However, in 2000, the young did not significantly increase their mass during the post-fledging period. In 2001, conditions were more favourable and body mass increased continuously. Further, in 2001, male post-fledglings were significantly heavier than female post-fledglings. Once having left the colony area (on average 18–23 days after fledging in 2000, and 14–16 days after fledging in 2001), post-fledgling body mass had still not reached adult body mass. The longer a juvenile stayed at the colony, the higher was its final body mass, which if acting as a threshold level may control departure time. Neither brood size nor hatching order affected post-fledging mass or period. In the unfavourable year 2000, when many individuals were found dead after fledging, fledging age but not fledging mass was found to be a predictor of post-fledging survival before departure: individuals fledging when older had a lower survival probability. Our results stress the importance of the post-fledging period for body mass increase and survival prior to departure. The variation in post-fledging mass growth between years and between the sexes is discussed with respect to parental effort and a possible selective provisioning of sons over daughters.     

Bioimpedance Identifies Body Fluid Loss after Exercise in the Heat: A Pilot Study with Body Cooling

Purpose

Assessment of post-exercise changes in hydration with bioimpedance (BI) is complicated by physiological adaptations that affect resistance (R) and reactance (Xc) values. This study investigated exercise-induced changes in R and Xc, independently and in bioelectrical impedance vector analysis, when factors such as increased skin temperature and blood flow and surface electrolyte accumulation are eliminated with a cold shower.

Methods

Healthy males (n = 14, 24.1±1.7 yr; height (H): 182.4±5.6 cm, body mass: 72.3±6.3 kg) exercised for 1 hr at a self-rated intensity (15 BORG) in an environmental chamber (33°C and 50% relative humidity), then had a cold shower (15 min). Before the run BI, body mass, hematocrit and Posm were measured. After the shower body mass was measured; BI measurements were performed continuously every 20 minutes until R reached a stable level, then hematocrit and Posm were measured again.

Results

Compared to pre-trial measurements body mass decreased after the run and Posm, Hct, R/H and Xc/H increased (p<0.05) with a corresponding lengthening of the impedance vector along the major axis of the tolerance ellipse (p<0.001). Changes in Posm were negatively related to changes in body mass (r = −0.564, p = 0.036) and changes in Xc/H (r = −0.577, p = 0.041).

Conclusions

Present findings showed that after a bout of exercise-induced dehydration followed by cold shower the impedance vector lengthened that indicates fluid loss. Additionally, BI values might be useful to evaluate fluid shifts between compartments as lower intracellular fluid loss (changed Xc/R) indicated greater Posm increase.     

Inter‐individual differences in rates of routine energy loss and growth in young‐of‐the‐year juvenile Atlantic cod

Inter‐individual differences in rates of routine (non‐feeding) metabolism and growth were evaluated in young‐of‐the‐year (YOY) juvenile Atlantic cod Gadus morhua . Rates of O₂ consumption, CO₂ production and ammonia (TAN) excretion were measured in 64, 25–43 mm standard length ( L _S) YOY growing at different rates (0·27–0·47 mm day⁻¹) in a common rearing tank. Parameter rates ( y ) increased allometrically ( y = a·M^b ) with increasing body mass ( M ) with b ‐values for O₂ production, CO₂ consumption and TAN excretion equal to 0·81, 0·89 and 0·56, respectively. In some cases, residuals from these regressions were significantly negatively correlated to fish growth rate. In no cases did residuals of parameter rates increase with increasing growth rate. These data suggest that, during unfed periods, relatively fast‐growing fish were more metabolically efficient than slower‐growing fish from the same cohort. The fish condition factor, derived from     , also significantly decreased with increasing growth rate. Results indicated differences in both the rates of routine energy loss and the patterns of growth allocation among YOY Atlantic cod. Since these physiological attributes were positively correlated with growth rate, they may be indicative of 'survivors' in field populations.     

Life history patterns in female moose (Alces alces): the relationship between age,body size,fecundity and environmental conditions

I examined the relationship between age, body size and fecundity in 833 female moose (Alces alces) from 14 populations in Sweden sampled during 1989–1992. Data on population density, food availability and climatic conditions were also collected for each population. Age and body mass were both significantly positively related to fecundity, measured as ovulation rate, among female moose. The relationship between the probability of ovulation and body mass was dependent on age with (1) a higher body mass needed in younger females for attaining a given fecundity, and (2) body mass having a stronger effect on fecundity in yearling (1.5 year) than in older (2.5 year) females. Thus, a 40 kg increase in yearling body mass resulted in a 42% increase in the probability of ovulation as compared to a 6% increase in older females. The lower reproductive effort per unit body mass, and the relatively stronger association between fecundity and body mass in young female moose compared to older ones, is likely to primarily represent a mechanism that trades off early maturation against further growth, indicating a higher cost of reproduction in young animals. In addition to age and body mass, population identity explained a significant amount of the individual variation in fecundity, showing that the relationship between body mass and fecundity was variable among populations. This variation was in turn related to the environment, in terms of climatic conditions forcing female moose living in relatively harsh/more seasonal climatic conditions to attain a 22% higher body mass to achive the same probability of multiple ovulation (twinning) as females living in climatically milder/less seasonal environments. The results suggests that the lower fecundity per unit body mass in female moose living in climatically harsh/more seasonal environments may be an adaptive response to lower rates of juvenile survival, compared to females experiencing relatively milder/less seasonal climatic conditions.     

Development of the solitary endoparasitoid Microplitis demolitor: host quality does not increase with host age and size

Abstract.  1. Many studies examining the relationship between host size, an index of host quality, and parasitoid fitness use development time and/or adult parasitoid size as currencies of fitness, while ignoring pre-adult mortality. Because the physiological suitability of the host may vary in different stages, sizes, or ages of hosts, a misleading picture of host quality may therefore be obtained in cases where fitness is based on only one or two developmental traits.
2. The development of the solitary koinobiont endoparasitoid Microplitis demolitor is examined in different larval age-classes of its host the soybean looper Pseudoplusia includens . Hosts were parasitised on days 1–8 after hatching from the egg, and development time, adult body size, and mortality of the parasitoid were compared.
3. A comparison of larval growth trajectories (using dry body mass) of M. demolitor revealed that parasitoid larvae attained over twice as much body mass in old hosts than in younger hosts. Similarly, adult parasitoid size at eclosion generally increased with host size, although parasitoids developing in smaller hosts lost a much lower proportion of mass between pupation and eclosion.
4. Overall egg-to-adult development was most rapid in intermediate-aged hosts, and longer in hosts at opposite ends of the age continuum. Moreover, parasitoid mortality varied non-linearly with host stage, and was generally higher in very young and older hosts.
5. Based on these results and other empirical data for koinobionts, it is argued that fitness functions in this group of parasitoids are not simply a positive function of host size or age, but instead may be distinctly dome-shaped, both patterns reflecting the degree of physiological and nutritional compatibility between the two organisms.     

NEW LIGHT ON THE SCALING OF METABOLIC RATE WITH THE SIZE OF ALGAE

The scaling of metabolic rate with the size of algae has been discussed and researched at length. The observation that algae usually have exponents b in the equation R = a· W ^{− b} (where R is the specific growth rate, W is the organism [cell] biomass, and a and b are constants) equal to or higher than the value of −0.25 for many other organisms is generally related to resource-saturated (maximal) values of R. Recent work has shown that the exponent b for light-limited growth is more negative than −0.25. This was predicted from considerations of the package effect in photon absorption, as modulated by the volume-specific pigment content of the cells, and the photosynthetic unit size. Further work is needed to extrapolate these findings to fluctuating light environments. This minireview puts the recent work into a broader context and suggests how further work could quantify the roles of optical thickness and of spatial and temporal variations in the radiation field in determining metabolic rates.     

Major life-history transitions by deterministic directional natural selection

For large-scale evolution on Earth there has been a directional change where simple self-replicators evolved into large organisms with high metabolic rates and long pre-reproductive periods. Associated with this increase there have been major life-history transitions from asomatic, non-senescing, haploid, and asexually reproducing organisms to somatic, senescing, diploid, and sexually reproducing organisms with male and female individuals. Using a game theoretical model, it is shown that this trajectory can be explained by deterministic natural selection as it arises from first principles of the self-replication process in mobile organisms. It is shown (i) that selection for an increase in the energetic state of the organism puts a direction to evolution, (ii) that selection by density-dependent competitive interactions can explain the major life-history transitions as a function of the energetic state of the organism, and (iii) that the two selection processes combined can explain an exponentially increasing body mass. It is also shown (iv) why, for the case with an increasing body mass, we may expect many life histories to evolve in accordance with the exponents of the body mass allometries, (v) that an upper constraint on the body mass and metabolic rate can induce an additional transition into eusocial communities, and (vi) that the evolutionary trajectory is likely reversible with backward evolution during periods of environmental crises.     

Effect of body size, temperature, and salinity on the routine metabolism of larval and juvenile spotted seatrout

Routine oxygen consumption rates of young spotted seatrout Cynoscion nebulosus (Sciaenidae) were measured over a range of temperatures (24, 28, 30 and 32° C) and salinities (5, 10, 20, 35 and 45). Larvae and juveniles, 4·1–39·5 mm standard length ( L _S), ranging several orders of magnitude in dry body mass were used to estimate the mass–metabolism relationship. Oxygen consumption (μl O₂ larva⁻¹ h⁻¹) scaled isometrically with body mass for larvae <5·8 mm L _S(phase I, slope = 1·04) and allometrically thereafter (phase II, slope = 0·78). The inflection in the mass–metabolism relationship coincided with the formation of the hypural plate and an increase in the relative tail size of larvae. Salinity did not have a significant effect on routine metabolism during phase I. Temperature and salinity significantly affected routine metabolism during phase II of the mass–metabolism relationship. The effect of salinity was temperature dependent, and was significant only at 30° C. Response surfaces describing the environmental influences on routine metabolism were developed to provide a bioenergetic basis for modelling environmental constraints on growth.     

Analysis of polymorphisms in the insulin-like growth factor 1 receptor (IGF1R) gene from Japanese quail selected for body weight

Insulin-like growth factor 1 receptor ( IGF1R ) is essential for the signalling of growth. In this study, we performed single nucleotide polymorphism (SNP) detection in the Japanese quail IGF1R coding region and an association study between SNPs and body weight in two lines (SS and LL) selected for large and small body weight. Of 21 SNPs obtained, a SNP at position AB292766:c.2293G>A led to the replacement of a valine with an isoleucine (V765I). The two lines were fixed for alternate alleles, with allele encoding valine fixed in the LL line. A significant effect of the SNP genotype was found on 10-week body weight ( P  < 0.01) and on 4- to 10-week and 6- to 10-week average daily gain ( P  < 0.05) in the F₂ family obtained from lines LL and SS. In six populations maintained in Japan or France, the frequency of allele encoding valine was higher than the allele encoding isoleucine.     

Decreases in motor unit firing rate during sustained maximal-effort contractions in young and older adults

Previous studies have suggested that older adults may be more resistant to muscular fatigue than young adults. We sought to determine whether motor unit firing rate might be a factor that determines the response to fatiguing exercise in young and older subjects. Motor unit recordings and muscular forces were obtained from the tibialis anterior (TA) muscle of 11 young and 8 older individuals. Maximal voluntary force was first measured during maximal-effort dorsiflexion contractions. Each subject then performed a series of 15 maximal isometric contractions, with each contraction lasting 30 s. A 10-s rest period separated the fatiguing contractions. As a result of the fatiguing exercise, both subject groups demonstrated a significant loss in maximal force. The force decline was less in the older adults (20.4%) than in the young adults (33.8%). As expected, prior to muscle fatigue, maximal firing rates in the TA muscle were greater in the young (28.1 ± 5.8 imp/s) than in the older adults (22.3 ± 4.8 imp/s). The decrease in motor unit firing rate with fatigue was also greater in the young adults (34.9%), than in the older adults (22.0%). These results suggest that the greater fatigue-resistance exhibited by older individuals might be explained by the fact that the decline in motor unit firing rate during fatigue is greater in young persons than it is in older adults.     

Energetics of locomotion and load carriage in the nectar feeding ant, Camponotus rufipes

Abstract.  To investigate if there is an energetic constraint influencing a nectar feeding ant's decision to come back to the nest with partial loads, the energetic costs of running and carrying a load in the ant Camponotus rufipes are measured. Metabolic rates of individuals are measured in a running tube respirometer while they are unladen and laden at 25 °C. Workers voluntarily collect a load of 6 µL of a 30% sucrose solution (mass = 6.8 mg), which results in an internal load of about 50% of the ant mass and is close to a full load for ants within this size range. The gross cost of unladen running is 264 J kg⁻¹ m⁻¹, while that of laden running is 225 J kg⁻¹ m⁻¹. The mass used to calculate the cost of laden running includes body mass of ant and load carried. Load carriage cost in C. rufipes foragers is calculated to be about 60% as much as body carriage per unit mass. Internal load carriage in C. rufipes is energetically cheaper compared with external carriage in other ant species. Such low carriage costs make it unlikely that the collection of partial crop loads in C. rufipes foragers is based on a minimization of foraging costs, as suggested for honeybees.     

Effects of temperature,salinity and body size on routine metabolism of coastal largemouth bass Micropterus salmoides

Routine metabolism (i.e. standard metabolism plus a low level of activity) of coastal largemouth bass Micropterus salmoides from Mobile‐Tensaw Delta, AL, U.S.A. was examined as a function of temperature (15, 20, 25 and 30° C), salinity (0, 4, 8 and 12) and body mass (range 24–886 g) using flow‐through respirometry. Functionally, a cubic relationship best described the effect of salinity on respiration; the magnitude of these effects increased with temperature and body mass. The best model predicted that specific respiration (mg O₂ g^?1 h^?1) at temperatures >20° C was lowest at salinities of 0·0 and 9·7, and elevated at 3·2 and 12·0; salinity had little to no effect at temperatures ≤20° C. Respiration increased exponentially with temperature, but when compared with previously published respiration rates for M. salmoides from northern latitudes, predicted respiration was higher at cool temperatures and lower at high temperatures. The reduced energetic cost near the isosmotic level (i.e. c. 9) may be an adaptive mechanism to tolerate periods of moderate salinity levels and may help explain why M. salmoides do not flee an area in response to increased salinity. Further, these results suggest that salinity has high energetic costs for coastal populations of M. salmoides and may contribute to the observed slow growth and small maximum size within coastal systems relative to inland freshwater populations.