Jonathan D. Allen

Size-specific predation on marine invertebrate larvae.

Predation on planktonic larval stages is frequently a major source of mortality for the offspring of benthic marine invertebrates. Mortality rate likely varies with larval size and developmental stage, but few experiments have measured how these factors affect predation rates. I used experimental reductions in egg size to test how variation in larval size affects the likelihood of predation during planktonic development. Blastomeres of the sand dollar Dendraster excentricus were separated at the two-cell stage to produce half-sized zygotes. Larvae resulting from this manipulation were tested for their susceptibility to predation relative to whole-sized siblings at four ages. Individuals from each size class were simultaneously presented as prey items to five predators (crab zoeae, crab megalopae, chaetognaths, solitary tunicates, and postlarval fish) in the laboratory. Four predators consumed significantly more half-sized larvae than whole-sized larvae, but one predator type (postlarval fish) consumed more whole-sized larvae. Predators that consumed more half-sized larvae also preferentially consumed younger larvae. In contrast, postlarval fish showed no significant prey preference based on larval age. These results suggest that assumptions of constant mortality rates during development should be modified to account for the effects of larval size and age.

The Peril of the Plankton

The pelagic environment is characterized by unevenly distributed resources and risks. Such unpredictability presents adaptive challenges to diverse planktonic organisms including the larvae of benthic marine invertebrates. Estimates of mortality during planktonic development are highly variable, ranging from 0% to 100% per day. Predation is considered a significant source of this mortality, but what explains the variability in estimates of the mortality of marine invertebrate larvae? While differential exposure of larval prey to predators may explain these widely variable estimates, adaptations that reduce vulnerability of marine larvae to predators may also be important. Although there are excellent reviews of predation upon larvae and of larval mortality and defenses, nearly 15 years have elapsed since these topics were formally reviewed. Here, we highlight recent advances in understanding the behavioral, chemical, and morphological defenses that larvae possess and assess their effectiveness in reducing the risk of predation. While recent work confirms that larval mortality is generally high, it also demonstrates that larvae can reduce their risk of predation in several ways, including: (1) temporarily escaping the benthos during vulnerable early stages, (2) producing chemical compounds that reduce palatability, (3) possessing morphological defenses such as spines and shells, and (4) exhibiting induced defensive responses whereby larvae can alter their behavior, morphology, and life histories in the presence of predators. Taken together, these studies indicate that marine invertebrate larvae possess a sophisticated suite of defensive phenotypes that have allowed them to persist in the life cycle of benthic invertebrates for eons.

Intermediate Modes of Larval Development: Bridging the Gap between Planktotrophy and Lecithotrophy

SUMMARY The extraordinary diversity of larval form and function in marine invertebrates has motivated many studies of development, ecology, and evolution. Among organisms with pelagic development via a larval stage, this diversity is often reduced to a dichotomy between two broad nutritional categories: planktotrophy and lecithotrophy. Despite the clear utility of the planktotrophy–lecithotrophy dichotomy to those interested in the history or consequences of life history patterns, it is also clear that a number of larval forms do not fit neatly into either of these general categories. Here we review studies of these intermediate larval forms, focusing on descriptions of larvae known as facultative feeders. Recent descriptions of larval development suggest that facultative feeders and other intermediate larval forms are not as rare as commonly assumed. We assess the importance of these forms for models of life‐history evolution and call for a more‐detailed and nuanced view of larval biology to account for their existence. Clearer knowledge of the phylogenetic distribution and frequency of occurrence of larvae that exhibit intermediate nutritional requirements is also essential for evaluating current ideas on evolutionary transitions between planktotrophy and lecithotrophy. Finally, intermediate larval types provide valuable and underutilized opportunities for testing hypotheses in the fields of larval ecology and the evolution of development.

Understanding the Effects of Low Salinity on Fertilization Success and Early Development in the Sand Dollar Echinarachnius parma

Free-spawning marine invertebrates that live near shore or in estuaries may experience reduced fertilization success during low-salinity events. Although several studies have documented reproductive failure at reduced salinity in estuarine animals, few have looked at whether developmental failure is due to a failure of fertilization or to a failure of fertilized eggs to cleave. In this study, we examined the effects of salinities ranging from 18 to 32 psu on fertilization success and early development in the sand dollar Echinarachnius parma. In addition to decoupling the effects of low salinity on fertilization from its effects on early cleavage, we also assessed whether eggs or sperm were the weak link in accounting for reproductive failure. We found that both fertilization and cleavage failed at salinities below about 22 psu but that development could be partially rescued by returning zygotes to full-strength seawater. We also found that sperm remained active and capable of fertilizing eggs even after being exposed to low salinities for 30 min.. Taken together, these results suggest that reproductive failure at low salinities in E. parma is due more to an inability of the fertilized eggs to cleave than to an inability of sperm to fertilize eggs.

How Does Metabolic Rate Scale With Egg Size? An Experimental Test With Sea Urchin Embryos

The consequences of changes in egg size for the development of marine invertebrates have been the subject of much theoretical and experimental work. Models that explore larval developmental modes in the context of maternal investment per offspring are often couched in an energetic framework, but the relationships between egg size and the energetics of larval development are poorly understood. We used blastomere separations to examine how experimental reductions in egg size affected (1) larval metabolic rate and (2) larval resistance to starvation. We found that separating blastomeres at the 2- and 4-cell stage resulted in average reductions of 50% and 75%, respectively, in larval metabolic rate. This suggests that, in an experimental context, mass-specific metabolic rate does not change with egg size. We also found that a 50% reduction in egg volume did not reduce the resistance of larvae to starvation when particulate food was withheld. This suggests that the material supplied to larvae in the egg is used primarily for construction of the larval body, rather than as a buffer against starvation or as a means of reducing reliance on exogenous fuel to sustain maintenance metabolism.

How do changes in parental investment influence development in echinoid echinoderms

SUMMARY Understanding the relationship between egg size, development time, and juvenile size is critical to explaining patterns of life‐history evolution in marine invertebrates. Currently there is conflicting information about the effects of changes in egg size on the life histories of echinoid echinoderms. We sought to resolve this conflict by manipulating egg size and food level during the development of two planktotrophic echinoid echinoderms: the green sea urchin, Strongylocentrotus droebachiensis and the sand dollar, Echinarachnius parma. Based on comparative datasets, we predicted that decreasing food availability and egg size would increase development time and reduce juvenile size. To test our prediction, blastomere separations were performed in both species at the two‐cell stage to reduce egg volume by 50%, producing whole‐ and half‐size larvae that were reared to metamorphosis under high or low food levels. Upon settlement, age at metamorphosis, juvenile size, spine number, and spine length were measured. As predicted, reducing egg size and food availability significantly increased age at metamorphosis and reduced juvenile quality. Along with previous egg size manipulations in other echinoids, this study suggests that the relationship between egg size, development time, and juvenile size is strongly dependent upon the initial size of the egg.

A novel report of hatching plasticity in the phylum Echinodermata.

Hatching plasticity occurs in response to a wide range of stimuli across many animal taxa, including annelids, arthropods, mollusks, and chordates. Despite the prominence of echinoderms in developmental biology and more than 100 years of detailed examination of their development under a variety of conditions, environmentally cued hatching plasticity has never been reported in the phylum Echinodermata. Here we report plasticity in the timing and stage of hatching of embryos of the sand dollar Echinarachnius parma in response to reductions in salinity. Embryos of E. parma increased their time to hatching more than twofold in response to ecologically relevant salinity reductions, while maintaining an otherwise normal developmental schedule. Embryos that experienced the greatest delay in hatching time emerged from the fertilization envelope as four-arm pluteus larvae rather than hatching as blastulae or early gastrulae. Salinity manipulations across multiple male-female pairs indicated high variability in hatching time both within and among clutches, suggesting significant intraspecific variation in developmental responses to salinity.

Environmental Induction of Polyembryony in Echinoid Echinoderms

Polyembryony, or the production of multiple offspring from a single zygote, is a widespread phenomenon in the animal kingdom. Various types of polyembryony have been described in arthropods, bryozoans, chordates, cnidarians, echinoderms, and platyhelminthes. We describe the induction of polyembryony in embryos of the sand dollar Echinarachnius parma and the pencil urchin Eucidaris tribuloides in response to elevated temperature and reduced salinity. Data on the environmental variation in temperature and salinity that normally occurs during the spawning season, combined with the range of laboratory conditions over which polyembryony was induced, suggest that polyembryony may occur frequently in these species under natural conditions. We tested an additional two species of echinoids for similar responses, but found little evidence for polyembryony in the green urchin Strongylocentrotus droebachiensis or the variegated urchin Lytechinus variegatus, suggesting that polyembryony is not a universal response of echinoids to fluctuations in temperature and salinity. The unexpected developmental changes that we observed in response to present-day fluctuations in temperature and salinity suggest that ongoing and future environmental shifts may drive substantial changes in marine invertebrate developmental patterns, and that these changes will be different across taxa.