Emily Carrington

Drag and dislodgment of an intertidal macroalga: consequences of morphological variation in Mastocarpus papillatus Kützing

Abstract Survival of intertidal macroalgae depends on their ability to withstand the large hydrodynamic forces generated by breaking waves, an ability that may be a function of both the morphology and size of the plant. Mastocarpus papillatus Kutzing is an intertidal red alga that exhibits a broad range of morphologies varying in papillar length and density, thallus thickness, and degree of branching. Drag was measured in a flow tank on single female gametophyte thalli spanning a broad range of morphologies and sizes. The drag coefficients of M. papillatus are highly variable, but this variation decreases at high water velocities (3–4 m · s−1). Other intertidal macroalgae have similar ranges of drag coefficients at high water velocities. Regression analysis indicates that drag force is primarily determined by the planform area of the thallus and is not strongly influenced by morphology. The diameter of stipes (where mechanical failure most often occurs) of mature thalli do not increase in proportion to the area supported, suggesting that thalli in habitats with heavy wave action may be size-limited regardless of their morphology. Calculations predict that maximum thallus size may be limited by water velocities that occur on exposed coasts.

Ecological genetics in the North Atlantic: environmental gradients and adaptation at specific loci.

The North Atlantic intertidal community provides a rich set of organismal and environmental material for the study of ecological genetics. Clearly defined environmental gradients exist at multiple spatial scales: there are broad latitudinal trends in temperature, meso-scale changes in salinity along estuaries, and smaller scale gradients in desiccation and temperature spanning the intertidal range. The geology and geography of the American and European coasts provide natural replication of these gradients, allowing for population genetic analyses of parallel adaptation to environmental stress and heterogeneity. Statistical methods have been developed that provide genomic neutrality tests of population differentiation and aid in the process of candidate gene identification. In this paper, we review studies of marine organisms that illustrate associations between an environmental gradient and specific genetic markers. Such highly differentiated markers become candidate genes for adaptation to the environmental factors in question, but the functional significance of genetic variants must be comprehensively evaluated. We present a set of predictions about locus-specific selection across latitudinal, estuarine, and intertidal gradients that are likely to exist in the North Atlantic. We further present new data and analyses that support and contradict these simple selection models. Some taxa show pronounced clinal variation at certain loci against a background of mild clinal variation at many loci. These cases illustrate the procedures necessary for distinguishing selection driven by internal genomic vs. external environmental factors. We suggest that the North Atlantic intertidal community provides a model system for identifying genes that matter in ecology due to the clarity of the environmental stresses and an extensive experimental literature on ecological function. While these organisms are typically poor genetic and genomic models, advances in comparative genomics have provided access to molecular tools that can now be applied to taxa with well-defined ecologies. As many of the organisms we discuss have tight physiological limits driven by climatic factors, this synthesis of molecular population genetics with marine ecology could provide a sensitive means of assessing evolutionary responses to climate change.

The hydrodynamic effects of shape and size change during reconfiguration of a flexible macroalga

SUMMARY Rocky intertidal organisms experience large hydrodynamic forces due to high water velocities created by breaking waves. Flexible organisms, like macroalgae, often experience lower drag than rigid organisms because their shape and size change as velocity increases. This phenomenon, known as reconfiguration, has been previously quantified as Vogels E, a measure of the relationship between velocity and drag. While this method is very useful for comparing reconfiguration among organisms it does not address the mechanisms of reconfiguration, and its application to predicting drag is problematic. The purpose of this study was twofold: (1) to examine the mechanisms of reconfiguration by quantifying the change in shape and size of a macroalga in flow and (2) to build a mechanistic model of drag for reconfiguring organisms. Drag, frontal area and shape of the intertidal alga Chondrus crispus were measured simultaneously in a recirculating flume at water velocities from 0 to ∼2 m s–1. Reconfiguration was due to two separate mechanisms: whole-alga realignment (deflection of the stipe) at low velocities (<0.2 m s–1) and compaction of the crown (reduction in frontal area and change in shape) at higher velocities. Change in frontal area contributed more to drag reduction than change in drag coefficient. Drag coefficient and frontal area both decrease exponentially with increasing water velocity, and a mechanistic model of drag was developed with explicit functions to describe these changes. The model not only provides mechanistic parameters with which to compare reconfiguration among individuals and species, but also allows for more reliable predictions of drag at high, ecologically relevant water velocities.

Fracture mechanics and the survival of wave-swept macroalgae

Abstract Wave-swept macroalgae are constructed from materials which are brittle compared to most biological structural materials. As a consequence, these plants are susceptible to breakage when they receive a sharp-ended surface injury. Field tests indicate that injuries such as razor cuts can result in rapid mortality even under benign surf conditions. However, because algal blade material is highly extensible, it allows for a rounding of the apex of a surface flaw, resulting in a substantial lowering of the stress concentration in the material. For all but the most sharply ended initial cracks, the rounding of the flaw is sufficient to make the local stress concentration the limiting factor in fracture. In this fashion macroalgal blades manage largely to avoid the dire consequences of being constructed from brittle materials.

Seasonal variation in mussel byssal thread mechanics

SUMMARY The blue mussel, Mytilus edulis, attaches itself to the substrate by producing a radially arranged complex of collagenous byssal threads. The strength of byssal attachment, or tenacity, has been shown to vary seasonally on Rhode Island shores, increasing twofold in spring in comparison with fall. It was previously assumed that this seasonality was due to increased thread production following periods of increased wave action; however, recent findings do not support this view. As an alternate hypothesis, this study evaluates the contribution of seasonal changes in the material properties of byssal threads to an annual cycle in mussel attachment strength. Tensile mechanical tests were performed seasonally, on both newly produced threads and on threads outplanted in the field for up to nine weeks. Threads produced in spring were over 60% stronger and 83% more extensible than threads produced in all other seasons. The mechanical integrity of byssal threads also deteriorated over time in spring and summer. These results suggest that reduced attachment strength in fall reflects the production of inferior quality threads following a period of increased decay. Here, we propose a new scheme where variation in byssal thread material properties, rather than quantity, explains the seasonal pattern in attachment strength observed on Rhode Island shores.

Seasonal influence of wave action on thread production in Mytilus edulis.

SUMMARY The blue mussel Mytilus edulis maintains a strong attachment to the substrate in high energy environments by producing byssal threads. On the shores of Rhode Island, USA, mussel attachment strength increases twofold in spring compared to that in the fall. While many factors could influence attachment strength (temperature, food supply, predator cues, etc.), it has been proposed that the variation observed is primarily due to increased thread production during winter and spring in response to increased wave action. This study evaluates the influence of three aspects of wave action on the thread production of M. edulis. Mussels were exposed to flow, acceleration and byssal loading stimuli and the subsequent number of byssal threads produced in the laboratory was monitored. Increased flow elicited the strongest response, significantly decreasing thread production in mussels. This result was confirmed in flume experiments exposing mussels to a range of flows, with reduced thread production above 15 cm s–1. The influence of both acceleration and byssal loading was sporadic and inconsistent across seasons. Surprisingly, overall thread production in the laboratory was lowest in winter, a time when mussels typically peak in attachment. A similar seasonal pattern was observed in field assays, with high thread production during periods of elevated temperature, reduced wave action, and high reproductive condition. These results suggest that seasonal variation in attachment strength does not reflect increased thread production in response to wave action, and that other possible factors, such as seasonal variability in both the material properties of byssal threads and thread decay rates, warrant further investigation.

LIFE HISTORY PHASES AND THE BIOMECHANICAL PROPERTIES OF THE RED ALGA CHONDRUS CRISPUS (RHODOPHYTA)

Chondrus crispus Stackhouse alternates between two isomorphic life history phases that differ in cell‐wall phycocolloid composition. It has been long hypothesized that the gametophyte, with strong‐gelling kappa‐type carrageenans, is mechanically superior to the tetrasporophyte, with nongelling lambda‐type carrageenans, which could contribute to the observed gametophytic dominance in many wave‐swept environments. Standard mechanical tests were performed on distal tissues of C. crispus sampled from a range of environments in Narragansett Bay, Rhode Island, using a tensometer equipped with a video extensometer. Life history phase was by far the most important determinant of mechanical properties, whereas environmental factors had only modest influence (vertical distribution) or no effect (exposure); gametophytic distal tissues were 43% stronger, 21% more extensible, and 21% stiffer than tetrasporophytic distal tissues. However, the superior strength of gametophytic tissues was not evident at the stipe/holdfast junction (where breakage typically occurs), and the two phases were equally susceptible to dislodgment by a given force. The primary ecophysiological role of carrageenans in C. crispus may not be the provision of a structure to resist wave action.

Interspecific Comparison of the Mechanical Properties of Mussel Byssus

Byssally tethered mussels are found in a variety of habitats, including rocky intertidal, salt marsh, subtidal, and hydrothermal vents. One key to the survival of mussels in these communities is a secure attachment, achieved by the production of byssal threads. Although many studies have detailed the unique biomechanical properties of byssal threads, only a few prevalent species have been examined. This study assesses the variation in the mechanical properties of byssus in a broad range of mussel species from diverse environments, including intertidal and subtidal Mytilus edulis, Modiolus modiolus, Geukensia demissa, Bathymodiolus thermophilus, and Dreissena polymorpha. A tensometer was used to measure quasi-static and dynamic mechanical properties of individual threads, and several aspects of morphology were quantified. The results indicate that thread mechanical properties vary among mussel species, and several novel properties were observed. For example, of the species examined, D. polymorpha threads were the strongest, stiffest, least resilient, and fastest to recover after partial deformation. Threads of M. modiolus were characterized by the presence of two distinct yield regions prior to tensile failure. This comparative study not only provides insight into the ecological limitations and evolution of mussels, but also suggests new models for the design of novel biomimetic polymers.

The Ecomechanics of Mussel Attachment: From Molecules to Ecosystems

Abstract One aspect of the physiological ecology of intertidal organisms is their mechanical design, which can be explored at many hierarchical levels, from molecules to ecosystems. Mechanical structures, as with any other physiological feature, require energy to construct and maintain, are subject to manufacturing and evolutionary constraints, and influence ecological performance. This contribution focuses on the ecomechanics of mussel attachment, which contributes to the competitive dominance of mussels on many wave-swept shores. Examples are presented to illustrate the hierarchical nature of mussel attachment, how levels of the hierarchy are interrelated, and where gaps in our knowledge remain. For example, water motion generates forces that mechanically deform byssal threads, but may also enhance the rate at which threads subsequently restore their original toughness. Furthermore, the ability of mussels to sense and respond to changes in their flow environment by producing a stronger attachment may be subject to physiological constraints, which in turn may have important consequences for the ecological response of mussels to shifts in wave climate. Thus an integrative approach to the study of byssal attachment is needed to fully understand this important aspect of the physiological ecology of mussels on rocky intertidal shores.

Mussel attachment on rocky shores: the effect of flow on byssus production

Mussels rely on a strong byssal attachment to persist in a range of habitats with differing rates of water flow. Recent studies, however, suggest that the ability of one mussel species to sense and respond adaptively to the flow in its environment is limited under even modest flow conditions because the process of byssal thread formation is disrupted. This study extends these findings to four mussel species, Mytilus trossulus, M. galloprovincialis, M. californianus, and Modiolus modiolus. Collectively, the response of byssal thread formation decreased with rates of flow above ∼25 cm/s and the critical flow threshold was estimated to be <50 cm/s. How can mussels persist on shores where flow is an order of magnitude higher? Using a combination of techniques for measuring flow, velocity profiles were obtained above and within mussel aggregations in the laboratory and in the field. Flow was greatly reduced within mussel aggregations, ranging from 0.1% to 10% of free-stream velocity. These results suggest one key to the success of mussels in habitats with high rates of flow is the ability to form aggregations that ameliorate flows to a level that is conducive to byssal thread formation.