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ABSTRACT Organisms are subject to the laws of physics, so comparative biomechanics is a powerful approach for identifying basic principles that apply across taxa of how morphology affects performance of mechanical functions such as locomotion, feeding or resisting damage. Journal of Experimental Biology has been a leading journal for decades in publishing studies revealing such basic biomechanical principles. However, field studies of the physical environment, ecological interactions and life-history strategies of organisms reveal which aspects of their biomechanical performance are important to their success in different types of natural habitats, and thus enable us to design ecologically relevant laboratory experiments to understand biomechanical function. Because the fitness consequences of differences in morphology are affected by the biological and physical environment, biomechanics can be used to identify how physical constraints on the performance of organisms with different body plans in variable environments can affect evolution. I illustrate these points with examples from the literature that show how the biomechanical consequences of morphology depend on the ecology of the organisms. Knowledge of the temporal patterns of interactions of organisms with their physical and biological environments is essential for understanding their functional morphology as it changes during ontogeny, and it reveals constraints on their evolution. 

Microscopic sessile suspension feeders live attached to surfaces and, by consuming bacteria-sized prey and by being consumed, they form an important part of aquatic ecosystems. Their environmental impact is mediated by their feeding rate, which depends on a self-generated feeding current. The feeding rate has been hypothesized to be limited by recirculating eddies that cause the organisms to feed from water that is depleted of food particles. However, those results considered organisms in still water, while ambient flow is often present in their natural habitats. We show, using a point-force model, that even very slow ambient flow, with speed several orders of magnitude less than that of the self-generated feeding current, is sufficient to disrupt the eddies around perpendicular suspension feeders, providing a constant supply of food-rich water. However, the feeding rate decreases in external flow at a range of non-perpendicular orientations due to the formation of recirculation structures not seen in still water. We quantify the feeding flow and observe such recirculation experimentally for the suspension feeder Vorticella convallaria in external flows typical of streams and rivers. 

The resistance of macroalgae to hydrodynamic forces imposed by ambient water motion depends in part on the mechanical properties of their tissues. In wave‐swept habitats, tissues are stretched (strained) at different rates as hydrodynamic forces change. Previous studies of mechanical properties of macroalgal tissues have used either a single strain rate or a small range of strain rates. Therefore, our knowledge of the mechanical properties of macroalgae is limited to a narrow fraction of the strain rates that can occur in nature. In addition, although mechanical properties of macroalgal tissues change with age, the effect of age on the strain‐rate dependence of their mechanical behavior has not been documented.

Using the kelpEgregia menziesii, we measured how high strain rate (simulating wave impingement) and low strain rate (simulating wave surge) affected mechanical properties of frond tissues of various ages.

Stiffness of tissues of all ages increased with strain rate, whereas extensibility was unaffected. Strength and toughness increased with strain rate for young tissue but were unaffected by strain rate for old tissue.

Young tissue is weaker than old tissue and, therefore, the most susceptible to breakage from hydrodynamic forces. The increased strength of young tissue at high strain rates can help the frond resist breaking when pulled rapidly during wave impingement, when hydrodynamic forces are largest. Because breakage of young tissue can remove a frond’s meristem and negatively impact the survival of the whole kelp, strain‐rate dependence of the young tissue’s strength can enhance kelp’s survival.

 

Choanoflagellates, unicellular eukaryotes that can form multicellular colonies by cell division and that share a common ancestor with animals, are used as a model system to study functional consequences of being unicellular versus colonial. This review examines performance differences between unicellular and multicellular choanoflagellates in swimming, feeding, and avoiding predation, to provide insights about possible selective advantages of being multicellular for the protozoan ancestors of animals. Each choanoflagellate cell propels water by beating a single flagellum and captures bacterial prey on a collar of microvilli around the flagellum. Formation of multicellular colonies does not improve the swimming performance, but the flux of prey‐bearing water to the collars of some of the cells in colonies of certain configurations can be greater than for single cells. Colony geometry appears to affect whether cells in colonies catch more prey per cell per time than do unicellular choanoflagellates. Although multicellular choanoflagellates show chemokinetic behavior in response to oxygen, only the unicellular dispersal stage (fast swimmers without collars) use pH signals to aggregate in locations where bacterial prey might be abundant. Colonies produce larger hydrodynamic signals than do single cells, and raptorial protozoan predators capture colonies while ignoring single cells. In contrast, ciliate predators entrain both single cells and colonies in their feeding currents, but reject larger colonies, whereas passive heliozoan predators show no preference. Thus, the ability of choanoflagellate cells to differentiate into different morphotypes, including multicellular forms, in response to variable aquatic environments might have provided a selective advantage to the ancestors of animals.

 

Microbial eukaryotes, critical links in aquatic food webs, are unicellular, but some, such as choanoflagellates, form multicellular colonies. Are there consequences to predator avoidance of being unicellular vs. forming larger colonies? Choanoflagellates share a common ancestor with animals and are used as model organisms to study the evolution of multicellularity. Escape in size from protozoan predators is suggested as a selective factor favoring evolution of multicellularity. Heterotrophic protozoans are categorized as suspension feeders, motile raptors, or passive predators that eat swimming prey which bump into them. We focused on passive predation and measured the mechanisms responsible for the susceptibility of unicellular vs. multicellular choanoflagellates,Salpingoeca helianthica, to capture by passive heliozoan predators,Actinosphaerium nucleofilum, which trap prey on axopodia radiating from the cell body. Microvideography showed that unicellular and colonial choanoflagellates entered the predator's capture zone at similar frequencies, but a greater proportion of colonies contacted axopodia. However, more colonies than single cells were lost during transport by axopodia to the cell body. Thus, feeding efficiency (proportion of prey entering the capture zone that were engulfed in phagosomes) was the same for unicellular and multicellular prey, suggesting that colony formation is not an effective defense against such passive predators.