Marcin Czarnoleski

Can Optimal Resource Allocation Models Explain Why Ectotherms Grow Larger in Cold

Abstract Basically all organisms can be classified as determinate growers if their growth stops or almost stops at maturation, or indeterminate growers if growth is still intense after maturation. Adult size for determinate growers is relatively well defined, whereas in indeterminate growers usually two measures are used: size at maturation and asymptotic size. The latter term is in fact not a direct measure but a parameter of a specific growth equation, most often Bertalanffys growth curve. At a given food level, the growth rate in determinate growers depends under given food level on physiological constraints as well as on investments in repair and other mechanisms that improve future survival. The growth rate in indeterminate growers consists of two phases: juvenile and adult. The mechanisms determining the juvenile growth rate are similar to those in determinate growers, whereas allocation to reproduction (dependent on external mortality rate) seems to be the main factor limiting adult growth. Optimal resource allocation models can explain the temperature-size rule (stating that usually ectotherms grow slower in cold but attain larger size) if the exponents of functions describing the size-dependence of the resource acquisition and metabolic rates change with temperature or mortality increases with temperature. Emerging data support both assumptions. The results obtained with the aid of optimization models represent just a rule and not a law: it is possible to find the ranges of production parameters and mortality rates for which the temperature-size rule does not hold.

Scaling of metabolism in Helix aspersa snails: changes through ontogeny and response to selection for increased size.

SUMMARY Though many are convinced otherwise, variability of the size-scaling of metabolism is widespread in nature, and the factors driving that remain unknown. Here we test a hypothesis that the increased expenditure associated with faster growth increases metabolic scaling. We compare metabolic scaling in the fast- and slow-growth phases of ontogeny of Helix aspersa snails artificially selected or not selected for increased adult size. The selected line evolved larger egg and adult sizes and a faster size-specific growth rate, without a change in the developmental rate. Both lines had comparable food consumption but the selected snails grew more efficiently and had lower metabolism early in ontogeny. Attainment of lower metabolism was accompanied by decreased shell production, indicating that the increased growth was fuelled partly at the expense of shell production. As predicted, the scaling of oxygen consumption with body mass was isometric or nearly isometric in the fast-growing (early) ontogenetic stage, and it became negatively allometric in the slow-growing (late) stage; metabolic scaling tended to be steeper in selected (fast-growing) than in control (slow-growing) snails; this difference disappeared later in ontogeny. Differences in metabolic scaling were not related to shifts in the scaling of metabolically inert shell. Our results support the view that changes in metabolic scaling through ontogeny and the variability of metabolic scaling between organisms can be affected by differential growth rates. We stress that future approaches to this phenomenon should consider the metabolic effects of cell size changes which underlie shifts in the growth pattern.

Cell size is positively correlated between different tissues in passerine birds and amphibians, but not necessarily in mammals

We examined cell size correlations between tissues, and cell size to body mass relationships in passerine birds, amphibians and mammals. The size correlated highly between all cell types in birds and amphibians; mammalian tissues clustered by size correlation in three tissue groups. Erythrocyte size correlated well with the volume of other cell types in birds and amphibians, but poorly in mammals. In birds, body mass correlated positively with the size of all cell types including erythrocytes, and in mammals only with the sizes of some cell types. Size of mammalian erythrocytes correlated with body mass only within the most taxonomically uniform group of species (rodents and lagomorphs). Cell volume increased with body mass of birds and mammals to less than 0.3 power, indicating that body size evolved mostly by changes in cell number. Our evidence suggests that epigenetic mechanisms determining cell size relationships in tissues are conservative in birds and amphibians, but less stringent in mammals. The patterns of cell size to body mass relationships we obtained challenge some key assumptions of fractal and cellular models used by allometric theory to explain mass-scaling of metabolism. We suggest that the assumptions in both models are not universal, and that such models need reformulation.

Cross-habitat differences in crush resistance and growth pattern of zebra mussels ( Dreissena polymorpha ): effects of calcium availability and predator pressure

We examined the growth pattern and shell strength of zebra mussels Dreissena polymorpha in eight European locations characterised by different survival rates, pH levels and calcium availability, testing whether trait variability can be attributed to anti-predator responses and how their expression might depend on mussel size and water chemistry. Differences in chemical conditions were unrelated to the cross-population gradient in survivorship, suggesting other agents such as predators as determinants of mussel survival. Increased population mortality was associated with production of stronger shells by mussels 8, 10 and 12 mm long, and with slower growth of 12- and 14-mm individuals. Shell strengthening was unrelated to growth rate across populations. Mortality correlated positively with Bertalanffys growth coefficient and negatively with asymptotic size. Chemical parameters were unrelated to growth patterns, but they had interactive effects with mortality on the crush resistance of 8- and 10-mm mussels. Under low-mortality conditions, higher calcium concentrations and lower pH stimulated production of stronger shells; the positive link between shell strength and population mortality was detectable across lower to medium calcium levels and medium to higher pH values. The results suggest adaptive responses to predation through increasing crush resistance and diversion of resources from growth to reproduction. They indicate that water chemistry can mediate induction of anti-predator responses, and that their efficacy changes over the mussel lifetime. We argue that a full consideration of the post-invasive polymorphism of zebra mussels must incorporate the interplay between environmental conditions and adaptive responses to mortality risk.

Substrate preference in settling zebra mussels Dreissena polymorpha

In a field experiment we compared recruitment of zebra mussels on two types of substrate surface, one flat and the other complex, imitating the heterogeneity of the surface between aggregated mussels. Concrete blocks, each presenting both types of substrate, were suspended horizontally or vertically in the water column along a lake shore. The density of recruits varied from 0 to 1.5 individuals/cm 2 across 92 experimental substrates. Density was not affected by substrate orientation; it was significantly higher on complex than on flat substrates (median 0.32 vs. 0.18 mussels/ cm 2 ). This indicates that besides the commonly suggested chemical cues, the complicated surface of mussel aggregates itself may elicit settling on conspecifics. We stress that gregariousness in Dreissena polymorpha may be an evolved antipredation strategy rather than a result of hyperproduction of larvae competing for scarce substrates.

How to Time Growth and Reproduction during the Vegetative Season: An Evolutionary Choice for Indeterminate Growers in Seasonal Environments

Indeterminate growers such as plants, mollusks, fish, amphibians, and reptiles are highly diversified with respect to the seasonal timing of growth and reproduction. Current life‐history theory does not offer a consistent view on the origin of this diversity. We use dynamic optimization to examine resource allocation in seasonal environments, considering that offspring produced at different times of the season have unequal future prospects. Reduction of these prospects during the season produced indeterminate growers that grew mostly after maturation, achieving large final body sizes. It also changed the optimal timing of growth and reproduction during a season, from grow‐first‐reproduce‐later, as usually predicted by life‐history theory, to the reproduce‐first‐grow‐later tactic; other tactics were produced by the interactive effects of winter survival and unequal offspring prospects. The results suggest that devaluation of offspring production provides conditions for the evolution of capital breeding, even in fully predictable seasonal environments. Thus, the unequal fate of newborns from different parts of a season may explain the origin of diversity of reproductive phenologies, growth patterns, and capital breeding in nature.

Flies developed small bodies and small cells in warm and in thermally fluctuating environments.

SUMMARY Although plasma membranes benefit cells by regulating the flux of materials to and from the environment, these membranes cost energy to maintain. Because smaller cells provide relatively more membrane area for transport, ectotherms that develop in warm environments should consist of small cells despite the energetic cost. Effects of constant temperatures on cell size qualitatively match this prediction, but effects of thermal fluctuations on cell size are unknown. Thermal fluctuations could favour either small or large cells; small cells facilitate transport during peaks in metabolic demand whereas large cells minimize the resources needed for homeoviscous adaptation. To explore this problem, we examined effects of thermal fluctuations during development on the size of epidermal cells in the wings of Drosophila melanogaster. Flies derived from a temperate population were raised at two mean temperatures (18 and 25°C), with either no variation or a daily variation of ±4°C. Flies developed faster at a mean temperature of 25°C. Thermal fluctuations sped development, but only at 18°C. An increase in the mean and variance of temperature caused flies to develop smaller cells and wings. Thermal fluctuations reduced the size of males at 18°C and the size of females at 25°C. The thorax, the wings and the cells decreased with an increase in the mean and in the variance of temperature, but the response of cells was the strongest. Based on this pattern, we hypothesize that development of the greater area of membranes under thermal fluctuations provides a metabolic advantage that outweighs the greater energetic cost of remodelling membranes.

Injured conspecifics alter mobility and byssus production in zebra mussels Dreissena polymorpha

In laboratory experiments we studied the effects of different concentrations of chemicals released by crushed conspecifics on zebra mussel mobility and byssogenesis (adhesive thread formation). In response to predation cues, zebra mussels showed reduced numbers of byssal threads, tendency for weaker byssal attachment, shorter distance travelled on sand and slower crawling speed, but duration of crawling did not change. Mussel mobility gradually decreased with increasing concentrations of predation cues. Our findings do not agree with the earlier suggestion that decreased mobility among zebra mussels exposed to predation cues results from acceleration of settlement and increased byssal production dynamics. The results do favour the view that zebra mussels slow their physiological processes in order to lower emissions of metabolites that disclose the location of prey to predators. This study suggests that zebra mussels sense different concentrations of predation cues, make chemosensory assessments of predation risk, and respond accordingly in order to reduce the cost of defences. When faced with predation risk, the zebra mussels seem to trade off resistance to predatory attacks to gain reduced risk of detection, but we argue that profitability of this strategy may depend on the likelihood of immediate attack.

The Temperature–Size Rule in Lecane inermis (Rotifera) is adaptive and driven by nuclei size adjustment to temperature and oxygen combinations ☆

The evolutionary implications of the Temperature-Size Rule (TSR) in ectotherms is debatable; it is uncertain whether size decrease with temperature increase is an adaptation or a non-adaptive by-product of some temperature-dependent processes. We tested whether (i) the size of the rotifer Lecane inermis affects fecundity in a way that depends on the combination of low or high temperature and oxygen content and (ii) the proximate mechanism underlying TSR in this species is associated with nuclei size adjustment (a proxy of cell size). Small-type and large-type rotifers were obtained by culturing at different temperatures prior to the experiment and then exposed to combinations of two temperature and two oxygen conditions. Fecundity was estimated and used as a measure of fitness. Nuclei and body sizes were measured to examine the response to both environmental factors tested. The results show the following for L. inermis. (i) Body size affects fecundity in response to both temperature and oxygen, supporting a hypothesis regarding the contribution of oxygen in TSR. (ii) Large individuals are generally more fecund than small ones; however, under a combination of high temperature and poor oxygen conditions, small individuals are more fecund than large ones, in accordance with a hypothesis of the adaptive significance of TSR. (iii) The body size response to temperature is realised by nuclei size adjustment. (iv) Nuclei size changes in response to temperature and oxygen conditions, in agreement with hypotheses on the cellular mechanism underlying TSR and on a contribution of oxygen availability in TSR. These results serve as empirical evidence for the adaptive significance of TSR and validation of the cellular mechanism for the observed response.

Seasonality in Offspring Value and Trade-Offs with Growth Explain Capital Breeding

The degree to which reproduction is based on reserves (capital breeding) and/or current acquisition (income breeding) drives extensive variation in organism life histories. In nature, pure income and capital breeding are endpoints of a continuum of diversity whose ultimate drivers are poorly understood. To study the adaptive value of capital and income breeding, we present an annual routine model of the life history of a perennial organism where reproductive value at birth varies seasonally. The model organisms allocate time and resources to growth, reproduction, and storage. Our model predicts that capital breeding is adaptive when timing of birth affects offspring reproductive value. The stronger the seasonality, the more time is dedicated to capital breeding and growth after maturation (indeterminate growth) instead of income breeding. This is because storage and growth are investments in future (residual) reproduction taken at times when offspring value is low. Storage is a short-term investment in offspring through capital breeding; growth is a long-term investment in reproductive potential. Because the modeled production rate increases less than linearly with body size, growth brings diminishing returns for larger organisms, favoring capital breeding. Building storage requires time, which limits growth opportunities, and we show for the first time that in seasonal environments, the degree of capital breeding is tightly linked to body size of indeterminate growers through allocation trade-offs.