Predicting the spread of aquatic invaders: insight from 200 years of invasion by zebra mussels.

Understanding factors controlling the introduction and spread of species is crucial to improving the management of both natural populations and introduced species. The zebra mussel, Dreissena polymorpha, is considered the most aggressive freshwater invader in the Northern Hemisphere, and is a convenient model system for invasion biology, offering one of the best aquatic examples for examining the invasion process. We used data on 553 of the 1040 glacial lakes in the Republic of Belarus that were examined for the presence of zebra mussels. We used these data to build, test, and construct modified models to predict the spread of this invader, including selection of important parameters that could limit the spread of this invader. In spite of 200 years of continuous invasion, by 1996, zebra mussels were found in only 16.8% of all lakes studied. Of those lakes without zebra mussels in 1996, 66% were predicted to be susceptible to invasion by zebra mussels in the future, and 33% were predicted to be immune to successful invasion due to their water chemistry. Eighty lakes free of zebra mussels in 1996 were reexamined from 1997 to 2008. Of these, zebra mussels successfully invaded an additional 31 lakes, all of which were classified initially as suitable for zebra mussels; none of the lakes previously classified as unsuitable were invaded. We used the Random Forests classification algorithm with 16 environmental variables to determine the most important factors that differed between invaded lakes and those lakes suitable for invasion that have not yet been invaded. Distance to the nearest infested lakes was found to be the most important variable, followed by the lake area, color, average depth, and concentration of chloride, magnesium, and bicarbonate. This study provides a useful approach for predicting the spread of an invader across a landscape with variable habitat suitability that can be applied to a variety of species and systems.

Preparing the Next Generation of Integrative Organismal Biologists.

Pursuing cutting edge questions in organismal biology in the future will require novel approaches for training the next generation of organismal biologists, including knowledge and use of systems-type modeling combined with integrative organismal biology. We link agendas recommending changes in science education and practice across three levels: broadening the concept of organismal biology to promote modeling organisms as systems interacting with higher and lower organizational levels; enhancing undergraduate science education to improve applications of quantitative reasoning and modeling in the scientific process; and K-12 curricula based on Next-Generation Science Standards emphasizing development and use of models in the context of explanatory science, solution design, and evaluating and communicating information. Out of each of these initiatives emerges an emphasis on routine use of models as tools for hypothesis testing and prediction. The question remains, however, what is the best approach for training the next generation of organismal biology students to facilitate their understanding and use of models? We address this question by proposing new ways of teaching and learning, including the development of interactive web-based modeling modules that lower barriers for scientists approaching this new way of imagining and conducting integrative organismal biology.

A systematic review of phenotypic plasticity in marine invertebrate and plant systems.

Marine organisms provide some of the most important examples of phenotypic plasticity to date. We conducted a systematic review to cast a wide net through the literature to examine general patterns among marine taxa and to identify gaps in our knowledge. Unlike terrestrial systems, most studies of plasticity are on animals and fewer on plants and algae. For invertebrates, twice as many studies are on mobile than sessile species and for both animals and plants most species are benthic intertidal zone taxa. For invertebrates, morphological plasticity is most common, while chemical plasticity is most common among algae. For algae, as expected, predators (inducible defences) are the primary cue for triggering plasticity. Surprisingly, for invertebrates the abiotic environment is the most common trigger for plasticity. Inducible defences in invertebrates have received great attention and predominate for a few well-studied species, which can bias perceptions; but, their predominance overall is not supported by the full data set. We also identified important research needs, including the need for data on non-temperate zone taxa, planned experiments to directly test the role of habitat variability and the prevalence of plasticity. We also need information on the lag time for induction of plastic traits, which is critical for determining the adaptive value of phenotypic plasticity. Studies of early life stages and studies that link plasticity to mechanisms that produce phenotypes are critically needed, as are phylogenetic comparative studies that can be used to examine responses of organisms to both short- and long-term change.

Changes in Food Selection through Ontogeny in Crassostrea gigas Larvae.

Bivalves are some of the most important suspension feeders in aquatic systems. Much research has been conducted on the feeding mechanisms of adult molluscan suspension feeders, but less is known about the feeding mechanisms of their larval stages. To date, the general consensus is that veligers are restricted to collecting particles 4-20 µm in size and that food selection is indiscriminate within this size range, but this hypothesis remains to be directly tested. Therefore, we experimentally assessed this assumption by quantifying microalgal particle capture rates for the larvae of the Pacific oyster (Crassostrea gigas) when fed five different microalgal species individually and in combination. We then tested whether factors such as cell size affected capture rate and consumption, as well as whether capture rate was affected by the presence of other microalgal species. We found evidence of food preference that was not simply a function of size or relative nutritional quality for C. gigas veligers. Further, we found that food selectivity changed through ontogeny. To our knowledge, the changes in selection that we observed through ontogeny have not been previously reported. Interestingly, there was also a sharp decrease in the variability among replicates in consumption rate as the larvae aged. Whether this is a function of velar structure or larval size remains to be tested. Our results suggest some underlying process resulting in certain species of microalgae being captured and consumed at significantly different rates than others.

A new organismal systems biology: how animals walk the tight rope between stability and change.

The amount of knowledge in the biological sciences is growing at an exponential rate. Simultaneously, the incorporation of new technologies in gathering scientific information has greatly accelerated our capacity to ask, and answer, new questions. How do we, as organismal biologists, meet these challenges, and develop research strategies that will allow us to address the grand challenge question: how do organisms walk the tightrope between stability and change? Organisms and organismal systems are complex, and multi-scale in both space and time. It is clear that addressing major questions about organismal biology will not come from "business as usual" approaches. Rather, we require the collaboration of a wide range of experts and integration of biological information with more quantitative approaches traditionally found in engineering and applied mathematics. Research programs designed to address grand challenge questions will require deep knowledge and expertise within subfields of organismal biology, collaboration and integration among otherwise disparate areas of research, and consideration of organisms as integrated systems. Our ability to predict which features of complex integrated systems provide the capacity to be robust in changing environments is poorly developed. A predictive organismal biology is needed, but will require more quantitative approaches than are typical in biology, including complex systems-modeling approaches common to engineering. This new organismal systems biology will have reciprocal benefits for biologists, engineers, and mathematicians who address similar questions, including those working on control theory and dynamical systems biology, and will develop the tools we need to address the grand challenge questions of the 21st century.

An integrated modeling approach to assessing linkages between environment, organism, and phenotypic plasticity.

Many of the most interesting questions in organismal biology, especially those involving the functional and adaptive significance of organismal characteristics, intrinsically transcend levels of biological organization. These organismal functions typically involve multiple interacting biological mechanisms. We suggest that subdisciplinary advances have led both to the opportunity and to the necessity to reintegrate knowledge into a new understanding of the whole organism. We present a conceptual framework for a modeling approach that addresses the functioning of organisms in an integrative way, incorporating elements from environments, populations, individuals, and intra-organismal dynamics such as physiology and behavior. To give substance to our conceptual framework, we provide a preliminary focal case study using phenotypic plasticity in the tooth morphology of snails in the genus Lacuna. We use this case study to illustrate ways in which questions about the evolution and ecology of organismal function intrinsically span all organizational levels. In this case, and in many others, quantitative approaches that integrate across mechanisms and scales can suggest new hypotheses about organismal function, and provide new tools to test those hypotheses. Integrative quantitative models also provide roadmaps for the large-scale collaborations among diverse disciplinary specialists that are needed to gain deeper insights into organismal function.

Effect of food on metamorphic competence in the model system Crepidula fornicata.

Food quality and quantity, as well as temperature, are all factors that are expected to affect rates of development, and are likely to be affected by expected climatic change. We tested the effect of a mixed diet versus a single-food diet on metamorphic competence in the emerging model species Crepidula fornicata. We then compared our results with other published studies on this species that examined time to metamorphic competence across a range of food concentrations and rearing temperatures. Ours was the only study to test the effects of single food versus a mixed diet on metamorphic competence for this species. Diet composition did not affect metamorphic competence or survivorship. Comparing results across studies, we found that the shortest time to metamorphic competence was typically found when the food availability per larva was the greatest, independent of rearing temperature. Unfortunately, some published studies did not include important metadata needed for comparison with other studies; these data included larval rearing density, food density, frequency of feeding, and rearing temperature. Mortality rates were not always reported and when reported were often measured in different ways, preventing comparison. Such metadata are essential for comparisons among studies as well as among taxa, and for the determination of generalizable patterns and evolutionary trends. Increased reporting of all such metadata is essential if we are to use scientific studies performed to their fullest potential.

Swimming speed of larval snail does not correlate with size and ciliary beat frequency.

Many marine invertebrates have planktonic larvae with cilia used for both propulsion and capturing of food particles. Hence, changes in ciliary activity have implications for larval nutrition and ability to navigate the water column, which in turn affect survival and dispersal. Using high-speed high-resolution microvideography, we examined the relationship between swimming speed, velar arrangements, and ciliary beat frequency of freely swimming veliger larvae of the gastropod Crepidula fornicata over the course of larval development. Average swimming speed was greatest 6 days post hatching, suggesting a reduction in swimming speed towards settlement. At a given age, veliger larvae have highly variable speeds (0.8-4 body lengths s(-1)) that are independent of shell size. Contrary to the hypothesis that an increase in ciliary beat frequency increases work done, and therefore speed, there was no significant correlation between swimming speed and ciliary beat frequency. Instead, there are significant correlations between swimming speed and visible area of the velar lobe, and distance between centroids of velum and larval shell. These observations suggest an alternative hypothesis that, instead of modifying ciliary beat frequency, larval C. fornicata modify swimming through adjustment of velum extension or orientation. The ability to adjust velum position could influence particle capture efficiency and fluid disturbance and help promote survival in the plankton.

Context-dependent impacts of a non-native ecosystem engineer, the Pacific oyster Crassostrea gigas.

The introduction of non-native species represents unprecedented large-scale experiments that allow us to examine ecological systems in ways that would otherwise not be possible. Invasion by novel ecological types into a community can press a system beyond the bounds normally seen and can reveal community interactions, local drivers and limits within systems that are otherwise hidden by coevolution and a long evolutionary history among local players, as well as local adaptation of species. The success of many invaders is attributed to their ability to thrive in a wide range of habitat types and physical conditions, setting the stage for direct examination of ecological impacts of a species across a range of habitat and community contexts. Bivalves are well-known ecosystem engineers, especially oysters, which are the target of wild-caught fisheries and aquaculture. The Pacific oyster, Crassostrea gigas, is grown worldwide for aquaculture, and is presently invading shores on virtually every continent. As a consequence, this non-native species is having large impacts on many systems, but the types of impacts are system specific, and greatly depend on substrate type, how physiologically stressful the environment is for intertidal zone species, and the presence of native engineering species. A novel type of engineering effect is identified for this non-native species, whereby it alters not only the physical environment, but also the thermal environment of the community it invades. The impacts of engineering by this non-native species will depend not only on whether it facilitates or inhibits species but also on the trophic level and ecological role of the species affected, and whether similar ecological types are found within the system.

Grand challenges in organismal biology.

A renaissance in organismal biology has been sparked by recent conceptual, theoretical, methodological, and computational advances in the life sciences, along with an unprecedented interdisciplinary integration with Mathematics, Engineering, and the physical sciences. Despite a decades-long trend toward reductionist approaches to biological problems, it is increasingly recognized that whole organisms play a central role in organizing and interpreting information from across the biological spectrum. Organisms represent the nexus where sub- and supra-organismal processes meet, and it is the performance of organisms within the environment that provides the material for natural selection. Here, we identify five "grand challenges" for future research in organismal biology. It is intended that these challenges will spark further discussion in the broader community and identify future research priorities, opportunities, and directions, which will ultimately help to guide the allocation of support for and training in organismal biology.

Legacies in life histories.

Complex life-histories are common in nature, have many important biological consequences, and are an important focal area for integrative biology. For organisms with complex life-histories, a legacy is something handed down from an ancestor or previous stage, and can be genetic, nutritional/provisional, experiential, as well as the result of random chance and natural variation in the environment. As we learn more about complex life-histories, it becomes clear that legacies are inexorably linked in the short- and long-term through ecology and evolution. Understanding the consequences and drivers of life-history patterns can therefore only be understood by considering all types of legacies and integrating legacies across the entire life cycle. Larry McEdward was a leader in the field of ecological physiology, and evolutionary ecology of marine invertebrate larvae with complex life-histories. Through his scientific work and publications, devotion to students, colleagues, family, and friends, Larry has left a lasting legacy that will impact the future development of the field of larval ecology and complex life-histories.

Ecological consequences of phenotypic plasticity.

Phenotypic plasticity is widespread in nature, and often involves ecologically relevant behavioral, physiological, morphological and life-historical traits. As a result, plasticity alters numerous interactions between organisms and their abiotic and biotic environments. Although much work on plasticity has focused on its patterns of expression and evolution, researchers are increasingly interested in understanding how plasticity can affect ecological patterns and processes at various levels. Here, we highlight an expanding body of work that examines how plasticity can affect all levels of ecological organization through effects on demographic parameters, direct and indirect species interactions, such as competition, predation, and coexistence, and ultimately carbon and nutrient cycles.

Are invasive species a major cause of extinctions?

The link between species invasions and the extinction of natives is widely accepted by scientists as well as conservationists, but available data supporting invasion as a cause of extinctions are, in many cases, anecdotal, speculative and based upon limited observation. We pose the question, are aliens generally responsible for widespread extinctions? Our goal is to prompt a more critical synthesis and evaluation of the available data, and to suggest ways to take a more scientific, evidence-based approach to understanding the impact of invasive species on extinctions. Greater clarity in our understanding of these patterns will help us to focus on the most effective ways to reduce or mitigate extinction threats from invasive species.