Intermediary metabolism and shell growth in the brachiopod Terebratalia transversa

Juvenile Terebratalia transversa (Brachiopoda) metabolize carbohydrates in the anterior-most marginal mantle at a rate of 0.46 μM glucose/g/hr (in vitro incubation of mantle in C¹⁴-glucose in a carrying medium of 10^-3 M non-radioactive glucose). The rate declines to 0.18μM glucose/g/hr in full-grown specimens. Carbohydrate metabolism in the marginal (anterior-most) mantle averages approximately 3.7 times greater than metabolism in (a portion of the ‘posterior’) mantle situated between the coelomic canals and the marginal mantle. This ratio remains constant in specimens of all sizes (i.e. an ontogenetic trend in the ratio is absent at p≤ 0.05). Organic acids are not detectable within the mantle (HPLC techniques) even after simulated anoxia (N₂ bubbling during mantle incubation). Glucose metabolism in vitro declines in both the marginal and ‘posterior’ mantles during anoxia and the metabolic ratio between marginal/‘posterior’ mantles becomes 1/1. We found no difference (at p≤ 0.05) in mean metabolic activity or in sue-related metabolic trends among populations from depths ranging between mean sea level and 70 m. However, the activity within the ‘posterior’ mantle was more variable in specimens from 70 m than in those from shallower habitats (10 m - mean sea level). The size of the specimens analyzed was most variable in the groups obtained from the shallowest habitats and least variable at 70 m depth. Our results may help define the energetics of fossil as well as living brachiopod shell growth. Brachiopod shell growth is known to be very slow relative to that of bivalves and our results indicate that this is a result of the animals' slow metabolism. The inflation of the valves in T. transversa is, in part, a function of the high ratio of intermediary metabolism in the marginal vs‘posterior’ mantle (i.e. parallels the relative growth rates at the shell margin vs‘posterior’ areas). We found that the bivalve, Chlamys hastata, which is commonly associated with T. transversa, has a lower ratio of metabolic activities in the ventral/dorsal mantle areas than the brachiopod has in the anterior/posterior. The difference produces a flatter shell in the bivalve in accord with allometric principles. The higher metabolic rate in the marginal vs‘posterior’ brachiopod mantle and its more pronounced decline with anaerobiosis is reflected in the greater definition of growth increments in the outer shell layer. Our results do not support recent generalizations that correlate shell thickness of a wide variety of invertebrates inversely with metabolic rate. Growth rate as determined from width of shell growth increments is a better index of metabolic rate. Although the genetic basis of glucose metabolism is unknown, the observed metabolic variability is consistent with suggestions that populations of marine organisms living in stable offshore environments are genetically more variable but morphologically more uniform than populations from shallow water. Furthermore, our results support suggestions that bivalved molluscs and brachiopods are very different metabolically, but the data are neutral with respect to theories of competitive exclusion of the two taxa throughout geologic history.     

Continuous growth-line sequences in gastropod shells

Studies of gastropod shell growth at the level of fine growth layers are scarce, because coiling of gastropod shells hinders the observation of continuous growth series spanning across whorls. We propose here a new method to obtain continuous growth patterns of gastropod shells over whorls with Terebralia palustris (L.) as an example. Comparison of vertical and horizontal sections of the shell of this species reveals that growth patterns can be observed continuously for several whorls on the vertical section of the columella. In addition, an obvious tidal growth pattern preserved in this species enables us to trace its growth with a precision of 12.4 h and indicates that it takes about two years for a shell to grow from 3 cm to 9.5 cm in height and add 5 complete whorls.     

Shell decay rates of native and alien freshwater bivalves and implications for habitat engineering

1. Spent shells of bivalves can provide habitat for other organisms, as well as playing important roles in biogeochemical cycles. The amount of spent shell material that will accumulate at a site depends on rates of both shell production and decay, although the latter is rarely considered. 2. We measured the instantaneous decay rates of four species of freshwater bivalves across a range of sites in south‐eastern New York, and found that rates varied by more than 500‐fold across sites and species. 3. Differences in decay rates were related to water chemistry (Ca, pH, dissolved inorganic C), the presence of a current, and the size of the bivalve shell. 4. Combining these decay rates with estimates of shell production derived from the literature, we conclude that the Unionidae, Corbicula, and Dreissena are all capable of producing large accumulations (>10 kg dry mass m⁻²) of spent shells, while members of the Sphaeriidae probably rarely will produce such large accumulations. 5. Hence the replacement of native unionid bivalves by the alien Corbicula and Dreissena may have little effect on standing stocks of spent shells, unless the aliens invade sites where unionids are scarce or absent.     

CONTRASTING PATTERNS OF HERITABLE GEOGRAPHIC VARIATION IN SHELL MORPHOLOGY AND GROWTH POTENTIAL IN THE MARINE GASTROPOD BEMBICIUM VITTATUM: EVIDENCE FROM FIELD EXPERIMENTS

Similar phenotypes do not always imply similar genotypes. In species distributed over a broad latitudinal range, geographical variation in morphological and life-history traits may reflect very different relations between genotypic and environmental effects on these traits. Patterns of selection among latitudinally separated sites may minimize phenotypic differences in life-history traits but promote phenotypic differences in form. Thus, for example, latitudinal variation in temperature often leads to genetically based metabolic differences that minimize differences in growth rate among populations at different latitudes (countergradient variation). However, variation in habitat experienced by the same populations may promote genetically based differences in shell form (cogradient variation). Few attempts have been made to assess simultaneously such mosaic effects of natural selection on the genetic basis of variation in both morphological and life-history traits among geographically separated populations. I quantified the extent to which widely separated populations of the rocky shore marine gastropod Bembicium vittatum exhibited genetic differences in shell shape, shell pattern, and growth rate. Bembicium vittatum occurs naturally at only three widely separated locations on the Western Australian coast. Individuals were transplanted from all three locations to a latitudinally intermediate site, where they were released in different pairwise combinations and allowed to reproduce. F₁ offspring from crosses between same- or different-source parents were identified using allozyme markers. When grown in a common environment, offspring from same-source parents exhibited similar differences in shell shape and pattern, but dramatic differences in growth rates, compared to native populations. Genetic variation therefore exists for all three traits. Growth rates in the common environment were positively correlated with latitude of the source population, confirming the existence of countergradient variation for growth associated with metabolic compensation. In addition, for both shell shape and growth rate, hybrids exhibited phenotypes roughly midway between the same-source parents, suggesting that genetic differences have a large additive component. In contrast, when one parent had pigmented spots, the offspring also had spots, suggesting a strong dominance component to the genetic basis of shell pattern. Genetic differences therefore yield different morphological phenotypes but similar life-history phenotypes, among latitudinally distant populations, and confirm a pattern of mosaic evolution in B. vittatum.     

Sound Characteristics and Outcome of Contests in Male Croaking Gouramis (Teleostei)

A correlative study using similar-sized males of the croaking gourami Trichopsis vittata was carried out to investigate whether sound characteristics influenced winning and if relative fighting ability was assessed by acoustic signals. Pair-wise contests between males were decided using lateral displays (LD) and vocalization in 26 cases, whereas 66 fights escalated to the frontal display (FD) phase. Physical fighting (mouth wrestling) and injuries were rarely observed in this species. Winners were generally larger than their opponents, and this effect was more pronounced in non-escalated than in escalated contests. Sounds of fight winners had a higher sound pressure level and also a lower dominant frequency. Neither number of acoustic signals nor duration of lateral and frontal displays were predictors of contest outcome. Acoustic measures were highly correlated to body weight. These results indicate that traits correlated with RHP (such as sound pressure level and dominant frequency) were predictors of the outcome, while traits not correlated with size (such as number and duration of displays) did not influence winning. In accordance with the main prediction of assessment models, the contest duration (cost) increased with the decrease in asymmetry of body length as well as sound pressure level. No such relationships were found for weight and dominant frequencies in LD- and FD-contests. The present study indicates that morphological and sound characteristics influence winning in fish. Moreover, the results suggest that croaking gouramis settle conflicts without damaging combats by assessing asymmetries in different components of RHP such as body weight and length, which may reliably be signalled by acoustic and visual assessment signals.     

Normoxic and anoxic heat output of the freshwater bivalves Pisidium and Sphaerium

In fasting Pisidium amnicum and Sphaerium corneum, regular periods of behavioural and metabolic quiescence were shown to occur in the normoxic, constant environment of the flow-through chamber of a heat-flow microcalorimeter. The metabolic rate was suppressed to 7.5% of normal at 10° C and to 8.5–9.7% at 20° C for periods exceeding the period of active metabolism by a factor of 3.5 at 10° C and 8.3 at 20° C. The rate of heat output during normoxic quiescence was equal to that during environmental anoxia, suggesting spontaneous achievement of body anoxia by complete shell closure. The mass-specific integrated heat output during closure periods was independent of size. Parallel observations on clam behaviour suggested that metabolic quiescence coincided with shell closure, and bursts of heat flow with active ventilation. Shell closure was accompanied by pronounced bradycardia, down to 20% of the active rate. In a constant environment, the rhythmic quiescence is regulated by shell closure which is probably triggered by lack of food. Regular quiescence of fasting bivalves may conserve energy reserves considerably, the amount depending on the possible excretion rate of the end products, and the post-quiescence recovery costs, which were not measured. Heat output during the active period was close to the average metabolic rate found earlier for Sphaeriidae. However, all the values determined so far are likely to be underestimates of the natural metabolism because the effects of digestion and growth are not included.     

Alternative Models for Allozyme-Associated Heterosis in the Marine Bivalve Spisula Ovalis

Correlations between allozyme heterozygosity and fitness-related traits, especially growth, have been documented in natural populations of marine bivalves. However, no consistent pattern has been exhibited, because heterotic effects on size vary with age and individual growth parameters are generally unknown. No consensus has emerged on the genetic basis of allozyme-associated heterosis. The species studied here, Spisula ovalis, displays annual shell growth lines, which allows us to compute individual age and growth dynamics over the whole life span. Our morphological study was coupled to a protein electrophoresis study at seven polymorphic loci. While the maximum size gained is not related to heterozygosity, the age at half maximum size, t(1/2), is significantly negatively correlated with heterozygosity, indicating an heterotic effect on initial growth. The correlation between heterozygosity and size is expected to vanish when age increases, due to the form of the growth function. This decreasing correlation is consistent with previous studies. We compare the relative performances of five linear models to analyze the genetic basis of heterosis. Surprisingly, the largest part of variance in t(1/2) is due to additive effects, the overdominant components being much weaker. Heterosis is therefore due to general genomic effects rather than to local overdominance restricted to allozymes or small neighboring chromosomal segments. A significant dependence of individual heterotic contributions of the enzyme loci upon expected heterozygosities, rather than metabolic function, further supports the hypothesis of enzymes acting as markers. General genomic effects can hold only if allozyme heterozygosity is positively correlated with heterozygosity at fitness-related genes scattered throughout the genome. This hypothesis is supported here by heterozygosity correlations between enzymatic loci.     

Physiological components of growth differences between individual oysters (Crassostrea gigas) and a comparison with Saccostrea commercialis

Pacific oysters (Crassostrea gigas) of identical age from two genetically distinct lines, one fast growing and the other slow growing, were held at three levels of ration and analysed for physiological traits to explain differences in their rates of growth. The data supported three hypotheses; faster growth was associated with faster rates of consumption of food, reduced metabolic rate at maintenance (i.e., at zero growth), and reduced metabolic costs of growth. A comparison with the Sydney rock oyster, Saccostrea commercialis, based on similar experiments on the two species, indicated that faster growth of Pacific oysters depended on similar physiological differences; the mean metabolic costs of growth, however, were similar in the two species. It is suggested that a general model for genetically linked differences in the growth rate of bivalve molluscs will need to include the processes of metabolic control rather than relying solely on an analysis of the individual components of the energetics of growth.     

Appearance of morphological novelty in a hybrid zone between two species of land snail

On the small oceanic island of Chichijima, two endemic species of land snails, Mandarina mandarina and M. chichijimana, have discrete distributions separated by a hybrid zone. This study investigates the potential of hybridization as a source of morphological novelty in these snails. Mandarina mandarina possesses a shell with a higher whorl expansion rate and a smaller protoconch than M. chichijimana, relative to shell size. The number of whorls and shell size of M. mandarina do not differ from those of M. chichijimana, because the effect of higher expansion rate on number of whorls and size of the former is compensated for by its smaller protoconch. The whorl expansion rate and protoconch diameter of the individuals from the hybrid populations are intermediate or typical of either of the two species, and their average values show clinal changes along the hybrid zone. However, the hybrid populations include exceptionally high shells with many whorls and flat shells with few whorls, which are never found in the pure populations of either species. In addition, gradual increases in variance in shell height and number of whorls were found from the edges to the center of the hybrid zone. A combination of low expansion rate (typical of M. chichijimana) and a small protoconch (typical of M. mandarina) produces a shell with an extremely large number of whorls because of the geometry of shell coiling. However, the combination of high expansion rate and a large protoconch produces a shell with an extremely small number of whorls. Because of the correlation between the number of whorls and shell height, shells with an exceptional number of whorls possess an extraordinarily high or flat spire. Hybrids can inherit a mosaic of characters that, as they play out during growth, lead to novel adult morphologies. These findings emphasize the importance of hybridization as a source of morphological variation and evolutionary novelty in land snails.     

Low global sensitivity of metabolic rate to temperature in calcified marine invertebrates

Metabolic rate is a key component of energy budgets that scales with body size and varies with large-scale environmental geographical patterns. Here we conduct an analysis of standard metabolic rates (SMR) of marine ectotherms across a 70° latitudinal gradient in both hemispheres that spanned collection temperatures of 0–30 °C. To account for latitudinal differences in the size and skeletal composition between species, SMR was mass normalized to that of a standard-sized (223 mg) ash-free dry mass individual. SMR was measured for 17 species of calcified invertebrates (bivalves, gastropods, urchins and brachiopods), using a single consistent methodology, including 11 species whose SMR was described for the first time. SMR of 15 out of 17 species had a mass-scaling exponent between 2/3 and 1, with no greater support for a 3/4 rather than a 2/3 scaling exponent. After accounting for taxonomy and variability in parameter estimates among species using variance-weighted linear mixed effects modelling, temperature sensitivity of SMR had an activation energy (Ea) of 0.16 for both Northern and Southern Hemisphere species which was lower than predicted under the metabolic theory of ecology (Ea 0.2–1.2 eV). Northern Hemisphere species, however, had a higher SMR at each habitat temperature, but a lower mass-scaling exponent relative to SMR. Evolutionary trade-offs that may be driving differences in metabolic rate (such as metabolic cold adaptation of Northern Hemisphere species) will have important impacts on species abilities to respond to changing environments.     

Plant growth strategy determines the magnitude and direction of drought-induced changes in root exudates in subtropical forests

Root exudates are an important pathway for plant–microbial interactions and are highly sensitive to climate change. However, how extreme drought affects root exudates and the main components, as well as species-specific differences in response magnitude and direction, are poorly understood. In this study, root exudation rates of total carbon (C) and its components (e.g., sugar, organic acid, and amino acid) were measured under the control and extreme drought treatments (i.e., 70% throughfall reduction) by in situ collection of four tree species with different growth rates in a subtropical forest. We also quantified soil properties, root morphological traits, and mycorrhizal infection rates to examine the driving factors underlying variations in root exudation. Our results showed that extreme drought significantly decreased root exudation rates of total C, sugar, and amino acid by 17.8%, 30.8%, and 35.0%, respectively, but increased root exudation rate of organic acid by 38.6%, which were largely associated with drought-induced changes in tree growth rates, root morphological traits, and mycorrhizal infection rates. Specifically, trees with relatively high growth rates were more responsive to drought for root exudation rates compared with those with relatively low growth rates, which were closely related to root morphological traits and mycorrhizal infection rates. These findings highlight the importance of plant growth strategy in mediating drought-induced changes in root exudation rates. The coordinations among root exudation rates, root morphological traits, and mycorrhizal symbioses in response to drought could be incorporated into land surface models to improve the prediction of climate change impacts on rhizosphere C dynamics in forest ecosystems.     

Geographic variation and thermal plasticity shape salamander metabolic rates under current and future climates

Predicted changes in global temperature are expected to increase extinction risk for ectotherms, primarily through increased metabolic rates. Higher metabolic rates generate increased maintenance energy costs which are a major component of energy budgets. Organisms often employ plastic or evolutionary (e.g., local adaptation) mechanisms to optimize metabolic rate with respect to their environment. We examined relationships between temperature and standard metabolic rate across four populations of a widespread amphibian species to determine if populations vary in metabolic response and if their metabolic rates are plastic to seasonal thermal cues. Populations from warmer climates lowered metabolic rates when acclimating to summer temperatures as compared to spring temperatures. This may act as an energy saving mechanism during the warmest time of the year. No such plasticity was evident in populations from cooler climates. Both juvenile and adult salamanders exhibited metabolic plasticity. Although some populations responded to historic climate thermal cues, no populations showed plastic metabolic rate responses to future climate temperatures, indicating there are constraints on plastic responses. We postulate that impacts of warming will likely impact the energy budgets of salamanders, potentially affecting key demographic rates, such as individual growth and investment in reproduction.     

Growth rate constrain morphological divergence when driven by competition

Resource competition has been hypothesized to be important in driving divergence by natural selection. The effect of competition on morphological divergence and plasticity has however rarely been investigated. Since low growth rates might constrain morphological modulation and individual growth rates usually are negatively related to the intensity of competition, there might be a connection between competition, growth rate and morphological divergence. We performed an aquarium experiment with young-of-the-year Eurasian perch ( Perca fluviatilis L.) to investigate how individual growth rate affected morphological plasticity induced by contrasting habitat treatments. Furthermore, in a field study of 10 lakes we also related the degree of morphological differentiation between habitats to the intraspecific competitior biomass. In the aquarium experiment we found that morphological plasticity was growth rate dependent in that morphological differentiation between the habitat treatments was confined to high individual growth rates. In the field study we found that morphological differentiation between habitats decreased with increasing intraspecific competitior biomass. Since plasticity is hypothesized to be important in divergence and intraspecific biomass could serve as a proxy for the level of competition, we suggest that our results indicate that morphological divergence might be constrained during periods of intense intraspecific competition due to low growth rates. A possible scenario is that at low growth rates all energy available is used for metabolic maintenance and no surplus energy is therefore available for morphological modulation.     

The effect of size and age on depuration rates of diarrhetic shellfish toxins (DST) in mussels (Mytilus edulis L.)

Depuration or elimination of diarrhetic shellfish toxins (DST) was followed for 73 days in 1- and 2-year-old mussels. The age groups also differed in size, providing a broad approach to studying the effect of the differences in physiology accompanying the differences in size. Content of DST was analysed both on groups and individual mussels. Environmental variables were measured to evaluate their effect on depuration.We found no significant differences in elimination rate of DST between 1- and 2-year-old mussels under natural conditions. This suggests that size and age do not affect the elimination rate of the DST. The present study is the first study on the effect of age and size on the elimination rate of algal toxins in bivalves. The natural variations in food levels and temperature were not found to affect the elimination rate of DST.The digestive gland weights in the 1-year-old mussels increased four times while the DST content per individual decreased eight times. This demonstrated that dilution of toxins due to tissue growth could have an important contribution to declines in toxin concentrations. Changes in tissue mass are affected by environmental variables via growth or starvation, and when such changes lead to concentration or dilution of toxins this does not reflect the accumulation or removal of toxins from the tissues. We hence suggest that when evaluating the actual elimination capacity of the mussels, as in the present study, the total content of toxins per individual should be used, rather than toxin concentrations.The 1-year-old mussels had faster growth compared to the 2-year-old mussels in both total soft tissue and digestive glands. The mechanism of DST elimination is still unknown. If this process involves metabolism of the toxins, one could expect the rates of elimination to follow overall metabolic rates. However, the results from the present study suggest that large differences in growth rates, which also include difference in feeding and metabolic rates, do not affect the elimination rate of DST. Our results support the assumption that the depuration rates cannot be accelerated, even in artificial systems, as a cost-effective way to solve the problem with toxic mussels for the industry.     

Some morphological adaptations in freshwater bivalves

Savazzi, E. & Yao, P. 1992 04 15: Some morphological adaptations in freshwater bivalves. Lethaia , Vol. 25, pp. 195–209. Oslo. ISSN 0024–1164.
Several freshwater bivalves possess peculiar shell morphologies. An extension of the postero-dorsal shell margins above the hinge line evolved convergently in several unionids. This extension supplements the opening momentum of the ligament, but must be broken off periodically in order to allow further shell growth. Arconaia and Cuneopsis have evolved twisted commissure planes, comparable to those found in unrelated marine bivalves. In marine forms, byssus is believed to have played a fundamental role in the evolution of shell torsion. However, the twisted Unionidae do not possess a byssus in the adult stage, thus forcing us to re-evaluate our ideas on the adaptive value and evolution of shell torsion. Solenaia oleivora is apparently incapable of reburrowing and of retracting its foot within the shell. The foot may be functional as an anchor, and is perhaps involved in chemosynthesis by storing sulphur extracted as sulphide from the surrounding sediment. Other adaptations of freshwater bivalves include selective thickening of portions of the shell that enhance its stability, permanent anterior and posterior gapes, and oyster-like morphologies and shell structures. * Functional morphology, constructional morphology, burrowing, shell torsion, Mollusca, Bivalvia, Unionacea, Recent, Quaternary, People's Republic of China .     

Larval development and metamorphosis in Pleurobranchaea maculata, with a review of development in the notaspidea (Opisthobranchia)

Pleurobranchaea maculata is a carnivorous notaspidean that is common in New Zealand. This species produces small eggs (diameter 100 microm) and planktotrophic veligers that hatch in 8 d and are planktonic for 3 weeks before settling on biofilmed surfaces (14 degrees C). Larval development is known in detail for only two other notaspidean species, P. japonica and Berthellina citrina. In all three species of pleurobranchids, mantle and shell growth show striking differences from veligers of other opisthobranch taxa. In young veligers of pleurobranchids, the shell is overgrown by the mantle, new shell is added by cells other than those of the mantle fold, and an operculum does not form. Thus some "adult" traits (e.g., notum differentiation, mechanism of shell growth, lack of operculum) are expressed early in larval development. This suggests that apomorphies characteristic of adult pleurobranchids evolved through heterochrony, with expression in larvae of traits typical of adults of other clades. The protoconch is dissolved post-settlement and not cast off as occurs in other opisthobranch orders, indicating that shell loss is apomorphic. P. maculata veligers are atypical of opisthobranchs in having a field of highly folded cells on the lower velar surface, a mouth that is posterior to the metatroch, and a richly glandular, possibly chemodefensive mantle. These data indicate that notaspidean larvae are highly derived in terms of the novel traits and the timing of morphogenic events. Phylogenetic analysis must consider embryological origins before assuming homology, as morphological similarities (e.g., shell loss) may have developed through distinct mechanisms.     

Eggshell structure, mode of development and growth rate in birds

The shell of an egg contributes to successful embryogenesis in many ways, such as through protection, respiration and water exchange. The shell is also the major source of calcium for the development of high-calcium consuming organs, e.g. the skeleton, muscles and brain. Some studies show, moreover, that growth rate may play a fundamental role in the pattern of skeletal development in birds: the faster the growth the less ossified the skeleton is at hatching. We predicted, therefore, that slow (precocial) and fast (altricial) growing bird species should lay eggs encased in shells with different structures adapted to support different rates of calcium removal by developing embryos. We tested this prediction by comparing the fine structure of the inner eggshell surface (mammillary layer) from 36 bird species belonging to 18 orders ranging from Struthioniformes to Passeriformes. Using scanning electron microscopy, we compared the mammillary layer of both non-incubated eggs and eggs at the time of hatching, i.e., before and after embryonic development and the accompanying calcium removal. The results were consistent with the prediction, i.e., the number of mammillary tips per unit of surface area was associated with mode of development and growth rate. The number was higher, and calcium removal was also more extensive, in shells from precocial bird species than in shells from altricial bird species.     

Detecting shifts in diversification rates without fossils

Studies of shifts in diversification rates and adaptive radiations are difficult when there are no fossils because past events cannot be inferred. The phylogenies of recent species, however, allow one to infer the patterns of past diversifications. I present a new method for estimating the diversification rate of a lineage, provided that a phylogeny of recent species, constructed, for instance, with molecular data, is available. This method was inspired by survival models and takes into account species that are not included in detailed phylogenetic data, provided that approximate dates of origin of these species are known. Likelihood ratio tests and Akaike Information Criterion make it possible to test for differences in diversification among lineages or groups of lineages and, thus, to evaluate adaptive radiation hypotheses. The present modeling approach can easily be extended to include temporal variations in diversification rates. A simulation study showed that the method is statistically consistent, avoiding Type I and Type II errors, and that it is robust to periodic or random fluctuations in the speciation rate. An example is presented with a composite phylogeny of primates.