Robert D. Podolsky

Temperature and Water Viscosity: Physiological Versus Mechanical Effects on Suspension Feeding

Water viscosity is inversely related to temperature. This simple physical relation couples two potential influences on organism performance. Seawater viscosity was manipulated, with and without temperature, to distinguish the physiological and mechanical effects of temperature on suspension feeding by ciliated echinoderm larvae. Change in viscosity alone accounted for half of the decline in the feeding rate at lower temperature. High viscosity shifted ingestion toward larger particles, which suggests that viscosity affects particle capture as well as rates of water processing. Temperature-induced change in viscosity, therefore, impacts suspension feeding independently of physiology and has implications for many small-scale biological processes.

Integrating function across marine life cycles

Complex life cycles involve a set of discrete stages that can differ dramatically in form and function. Transitions between different stages vary in nature and magnitude; likewise, the degree of autonomy among stages enabled by these transitions can vary as well. Because the selective value of traits is likely to shift over ontogeny, the degree of autonomy among stages is important for understanding how processes at one life-history stage alter the conditions for performance and selection at others. We pose 3 questions that help to define a research focus on processes that integrate function across life cycles. First, to what extent do particular transitions between life-history stages allow those stages to function as autonomous units? We identify the roles that stages play in the life history, types of transitions between stages, and 3 forces (structural, genetic/epigenetic, and experiential) that can contribute to integration among stages. Second, what are the potential implications of integration across life cycles for assumptions and predictions of life-history theory? We provide 3 examples where theory has traditionally focused on processes acting within stages in isolation from others. Third, what are the long-term consequences of carryover of experience from one life cycle stage to the next? We distinguish 3 scenarios: persistence (effects of prior experience persist through subsequent stages), amplification (effects persist and are magnified at subsequent stages), and compensation (effects are compensated for and diminish at subsequent stages). We use these scenarios to differentiate between effects of a carryover of state and carryover into subsequent processes. The symposium introduced by our discussion is meant to highlight how discrete stages can be functionally coupled, such that life cycle evolution becomes a more highly integrated response to selection than can be deduced from the study of individual stages.

Evolution of egg target size: An analysis of selection on correlated characters

Abstract In broadcast‐spawning marine organisms, chronic sperm limitation should select for traits that improve chances of sperm‐egg contact. One mechanism may involve increasing the size of the physical or chemical target for sperm. However, models of fertilization kinetics predict that increasing egg size can reduce net zygote production due to an associated decline in fecundity. An alternate method for increasing physical target size is through addition of energetically inexpensive external structures, such as the jelly coats typical of eggs in species from several phyla. In selection experiments on eggs of the echinoid Dendraster excentricus, in which sperm was used as the agent of selection, eggs with larger overall targets were favored in fertilization. Actual shifts in target size following selection matched quantitative predictions of a model that assumed fertilization was proportional to target size. Jelly volume and ovum volume, two characters that contribute to target size, were correlated both within and among females. A cross‐sectional analysis of selection partitioned the independent effects of these characters on fertilization success and showed that they experience similar direct selection pressures. Coupled with data on relative organic costs of the two materials, these results suggest that, under conditions where fertilization is limited by egg target size, selection should favor investment in low‐cost accessory structures and may have a relatively weak effect on the evolution of ovum size.

Strange Floral Attractors: Pollinator Attraction and the Evolution of Plant Sexual Systems

Individual plants of hummingbird-pollinated Besleria triflora display two flower morphs: staminate flowers, which have shortened styles and do not produce fruit, and hermaphrodite flowers. Experiments with B. triflora indicate that pollinator attraction can drive the evolution of a dimorphic plant sexual system. In field-manipulated plants, visitation increased at large floral displays; however, pollen receipt increased only when staminate flowers were used to enlarge the display. Laboratory experiments showed that staminate flowers do not remove pollen from visiting pollinators, effectively concentrating outcross pollen onto stigmas of fertile flowers. A dimorphic sexual system is favored because the morphology of staminate flowers enhances their role in pollinator attraction.

Life-History Consequences of Investment in Free-Spawned Eggs and Their Accessory Coats

The optimal trade‐off between offspring size and number can depend on details of the mode of reproduction or development. In marine organisms, broadcast spawning is widespread, and external coats are a common feature of spawned eggs. Egg jelly coats are thought to influence several aspects of fertilization and early development, including the size of the target for sperm, fertilization efficiency, egg suspension time, polyspermy, embryo survival, and fecundity. These costs and benefits of investment in jelly result in trade‐offs that can influence optimal reproductive allocation and the evolution of egg size. I develop an optimization model that sequentially incorporates assumptions about the function of egg coats in fertilization. The model predicts large variation in coat size and limited variation in ovum size under a broad range of conditions. Heterogeneity among spawning events further limits the range of ovum sizes predicted to evolve under sperm limitation. In contrast, variation in larval mortality predicts a broad range of optimal ovum sizes that more closely reflects natural variation among broadcast‐spawning invertebrates. By decoupling physical and energetic size, egg coats can enhance fertilization, maintain high fecundity, and buffer the evolution of ovum size from variation in spawning conditions.

Integrating Development and Environment to Model Reproductive Performance in Natural Populations of an Intertidal Gastropod

Abstract Functional challenges can differ among life-history stages, yet performance at one stage may be linked to the outcome of performance at others. For example, adult performance, in terms of the location or timing of reproduction in response to environmental signals, can set conditions that affect the performance of developmental stages. In marine invertebrates, however, early performance has been studied primarily in the laboratory. I outline an integrative approach to the study of field reproductive performance in a marine gastropod that undergoes development in intertidal habitats. Embryos within gelatinous masses experience high variability in development temperature and frequent exposure to thermal stress. In laboratory experiments, developmental performance was measured as a function of maximum temperature (Tmax) experienced during fluctuations that mimicked field tidal profiles. Performance curves showed declines that coincided with temperature thresholds for heat shock protein (Hsp) expression, a signal of cellular stress. Application of laboratory results to field records of Tmax predicted large variation in the survival of embryos deposited on different days. Timing of field reproduction was non-random with respect to Tmax, suggesting that adults could help to buffer embryos from environmental stress. Embryo survival, however, was not predicted to benefit from the non-random pattern of adult reproduction. Adults may be constrained to respond to information that only weakly predicts conditions that embryos will experience. Studies that incorporate linkages between life cycle stages in the field may better reveal how performance capacities and constraints at one stage can influence performance and selection at others.

Developmental plasticity in Macrophiothrix brittlestars: are morphologically convergent larvae also convergently plastic?

The pluteus larval forms of sea urchins (echinoids) and brittlestars (ophiuroids) use an internal skeleton to project arms that bear a long ciliated band used in swimming and feeding. The length of this ciliated band influences rates of maximum food clearance for larvae of both echinoderm classes and affects rates of growth and development in the plankton. Phylogenetic and morphological evidence, however, tend to support the view that the pluteus morphologies of the two classes are independently derived. Studies with echinoplutei have shown that investment in skeletal growth and ciliated band length changes in response to food conditions, with poorly fed larvae investing more in growth of the larval skeleton and arms either absolutely or in relation to other larval or developing postlarval structures. We present evidence for similar plasticity of skeletal growth in ophioplutei. We examined four species in the brittlestar genus Macrophiothrix that spanned a 3.8-fold range in egg size. Sibling larvae in 14 male-female crosses were reared with high (H) or low (L) food rations, and measurements were recorded for five skeletal arm rods and three non-arm body dimensions. The expression of adaptive plasticity (significantly longer arms in L versus H cultures on a given day) was apparent for most crosses in M. koehleri, the species with the smallest egg size. In the single cross for M. longipeda, larvae from L cultures had longer arms for their body length or stomach width than did larvae from H cultures. In these cases, plasticity was similar in timing, persistence, and magnitude to previously published results from echinoplutei. If internal skeletons are independently derived in the two classes, then plasticity in the expression of this homoplastic trait may itself be homoplastic.

Variety is the Spice of Life Histories: Comparison of Intraspecific Variability in Marine Invertebrates

Life-history characteristics of marine invertebrates exhibit broad diversity across taxa as well as considerable variation within species. Although such variation is widely recognized, comparisons of the magnitude of variability as an outcome of evolutionary processes are relatively rare. Theory predicts, for example, that patterns of variability within and between clutches can arise as a consequence of population genetic structure, environmental variability, and the uncertainty of future ecological conditions. We review the strengths and weaknesses of several statistical methods for comparing variability across distributions, including Levenes test, use of the coefficient of variation in F-tests, and analysis of covariance. We then use four case studies from our own work and from the literature to illustrate adaptive patterns of variability related to metamorphosis, habitat differentiation, physiological stress, and life-history mode. These examples demonstrate the value of comparing variability for a range of questions associated with reproductive ecology, life-history biology, and genotype-by-environment interactions. We encourage researchers studying larval ecology and life-history evolution to explicitly consider the causes and consequences of variances in traits along with their means in models, experimental designs, analyses, and interpretations.

Photosynthesis Drives Oxygen Levels in Macrophyte- Associated Gastropod Egg Masses

Many aquatic animals deposit fertilized eggs in adherent clutches or gelatinous masses. Egg aggregation carries certain risks, including the potential for inadequate oxygen supply to embryos. Physical and biological conditions alter such risks. We examined the effects of light levels and associated photosynthetic organisms on the distribution of oxygen inside gelatinous egg masses of four temperate gastropod species. Egg masses of two species, the opisthobranchs Melanochlamys diomedea and Haminoea callidegenita, contained significant populations of diatoms but generally were not associated with macrophytes. Egg masses of the other two species, the opisthobranch Haminoea vesicula and the prosobranch Lacuna sp., occurred commonly on subtidal macrophytes and appeared not to contain significant populations of diatoms. In the laboratory, we used microelectrodes to measure oxygen levels inside masses exposed to alternating dark and light conditions; light level had an enormous influence on oxygen profiles in egg masses of all four species. Masses of H. vesicula and Lacuna sp., when experimentally separated from their macrophytes, showed only slight increases in oxygen upon light exposure, indicating that the main source of oxygen in situ was the macrophyte rather than associated microalgae. Our findings indicate that photosynthesis by macrophytes can drive large changes in internal oxygen profiles.

Holding On to a Shifting Substrate: Plasticity of Egg Mass Tethers and Tethering Forces in Soft Sediment for an Intertidal Gastropod

Staying attached at a favorable site can be a major challenge for organisms in flow. Meeting this challenge depends on properties of the attachment structure and substrate, the nature of fluid flow, and the ability to adjust attachment force in response to hydrodynamic conditions. A broad taxonomic range of adult stages use adhesion or suction to attach to hard substrates in intertidal habitats, which experience flow from waves and tidal currents. We address the unique challenges of attachment to soft sediment in reproductive structures deposited on tidal flats. Egg masses of the opisthobranch mollusc Melanochlamys diomedea are anchored to the sediment by a buried tether composed of gel and sediment. In the field, populations differed in absolute tethering force and tethering force per unit size (= tenacity). Population differences in tenacity persisted for egg masses oviposited under common conditions in the laboratory. Adults exposed to greater flow produced tethers with greater tenacity but without an increase in tether size. Tethers tended to fail by slippage rather than breakage, indicating that tethering force depends more on frictional interaction with sediment than on strength of the tether axis. These results suggest that adults respond to variation in risks of embryo dislodgment by adjusting the tethering properties of egg masses, and that these adjustments involve more than simple changes in tether length or mass.