Whole-organism responses to constant temperatures do not predict responses to variable temperatures in the ecosystem engineer Mytilus trossulus

Understanding and predicting responses of ectothermic animals to temperature are essential for decision-making and management. The thermal performance curve (TPC), which quantifies the thermal sensitivity of traits such as metabolism, growth and feeding rates in laboratory conditions, is often used to predict responses of wild populations. However, central assumptions of this approach are that TPCs are relatively static between populations and that curves measured under stable temperature conditions can predict performance under variable conditions. We test these assumptions using two latitudinally matched populations of the ecosystem engineer Mytilus trossulus that differ in their experienced temperature variability regime. We acclimated each population in a range of constant or fluctuating temperatures for six weeks and measured a series of both short term (feeding rate, byssal thread production) and long-term (growth, survival) metrics to test the hypothesis that performance in fluctuating temperatures can be predicted from constant temperatures. We find that this was not true for any metric, and that there were important interactions with the population of origin. Our results emphasize that responses to fluctuating conditions are still poorly understood and suggest caution must be taken in the use of TPCs generated under constant temperature conditions for the prediction of wild population responses.

Dreissenids’ breaking loose: differential attachment as a possible driver of the dominance shift between two invasive mussel species

Ponto-Caspian dreissenids are notorious freshwater invaders. Recently, widespread observations show a dominance shift from the early invader, Dreissena polymorpha, to its successor, Dreissena bugensis. These observations likely reflect congeneric species differences in physiological and behavioural traits. Here, we assessed the mussel attachment strength, attachment rate, and the mode of byssal failure as trait differences that could potentially contribute to dominance shifts. The attachment traits were measured in field and laboratory experiments. Fouling plates were deployed in the Rhine-Meuse river delta and dreissenids were collected and acclimatised in 60 L non-aerated freshwater tanks. Attachment strength was positively correlated with shell size. The attachment strength of D. bugensis was significantly greater compared to slower growing D. polymorpha individuals of a dreissenid field assemblage. This corresponded to the superior byssal thread morphology of D. bugensis (i.e. higher number and two times wider byssal threads). Moreover, our results indicated that byssal threads of D. bugensis are stronger than those of D. polymorpha, as the latter ruptured more often. Additionally, D. bugensis had a significantly lower attachment rate than D. polymorpha. Having a greater attachment strength gives D. bugensis an advantage when it comes to withstanding currents and predators. On the other hand, not being attached allows an individual to actively move around. This would allow them to move away from fast changing unfavourable environmental conditions. These attachment traits indicate competitive benefits for D. bugensis over D. polymorpha, therefore possibly contributing to the dominance shifts.

Trait strengthening in mussels.xlsx

<p>Plastic pollution is ubiquitous with increasing recognition of its direct effects on species’ fitness. Little is known, however, about its more subtle effects, including the influence of plastic pollution on the morphological, functional and behavioural traits of organisms that are central to their ability to withstand disturbances. Among the least obvious but most pernicious forms of plastic-associated pollution are the chemicals that leach from microplastics. Here, we investigate how such leachates influence species’ traits by assessing functional trait compensation across four species of intertidal mussels, through investigations of byssal thread production, movement and aggregation behaviour for mussels held in natural seawater or seawater contaminated by microplastic leachates.</p><p>Seuront, L., Nicastro, K.R., McQuaid, C.D. and Zardi, G.I., Microplastic leachates induce species‐specific trait strengthening in intertidal mussels. <i>Ecological Applications</i>, p.e2222. <a href="https://0-doi.org.wam.seals.ac.za/10.1002/eap.2222"><b>https://0-doi.org.wam.seals.ac.za/10.1002/eap.2222</b></a></p><p></p><p>Seuront, Laurent; Nicastro, Katy; McQuaid, Christopher; Zardi, Gerardo (2020), Trait strengthening in mussels, v2, Dataset, <a href="https://doi.org/10.5061/dryad.905qftthq">https://doi.org/10.5061/dryad.905qftthq</a></p><br><p></p>

Trait strengthening in mussels.xlsx

<p>Plastic pollution is ubiquitous with increasing recognition of its direct effects on species’ fitness. Little is known, however, about its more subtle effects, including the influence of plastic pollution on the morphological, functional and behavioural traits of organisms that are central to their ability to withstand disturbances. Among the least obvious but most pernicious forms of plastic-associated pollution are the chemicals that leach from microplastics. Here, we investigate how such leachates influence species’ traits by assessing functional trait compensation across four species of intertidal mussels, through investigations of byssal thread production, movement and aggregation behaviour for mussels held in natural seawater or seawater contaminated by microplastic leachates.</p><p>Seuront, L., Nicastro, K.R., McQuaid, C.D. and Zardi, G.I., Microplastic leachates induce species‐specific trait strengthening in intertidal mussels. <i>Ecological Applications</i>, p.e2222. <a href="https://0-doi.org.wam.seals.ac.za/10.1002/eap.2222"><b>https://0-doi.org.wam.seals.ac.za/10.1002/eap.2222</b></a></p><p></p><p>Seuront, Laurent; Nicastro, Katy; McQuaid, Christopher; Zardi, Gerardo (2020), Trait strengthening in mussels, v2, Dataset, <a href="https://doi.org/10.5061/dryad.905qftthq">https://doi.org/10.5061/dryad.905qftthq</a></p><br><p></p>

Force distribution and multiscale mechanics in the mussel byssus

The byssi of sessile mussels have the extraordinary ability to adhere to various surfaces and withstand static and dynamic loadings arising from hostile environmental conditions. Many investigations aimed at understanding the unique properties of byssal thread–plaque structures have been conducted and have inspired the enhancement of fibre coatings and adhesives. However, a systems-level analysis of the mechanical performance of the composite materials is lacking. In this work, we discuss the anatomy of the byssus and the function of each of the three components (the proximal thread portion, the distal thread portion and the adhesive plaque) of its structures. We introduce a basic nonlinear system of springs that describes the contribution of each component to the overall mechanical response and use this model to approximate the elastic modulus of the distal thread portion as well as the plaque, the response of which cannot be isolated through experiment alone. We conclude with a discussion of unresolved questions, highlighting areas of opportunity where additional experimental and theoretical work is needed. This article is part of the theme issue ‘Transdisciplinary approaches to the study of adhesion and adhesives in biological systems’.

Native versus invasive crab effluent effects on byssal thread production in the mussel, Mytilus trossulus (Gould, 1950)

Mussels have evolved many adaptations to protect themselves, including the production of byssal threads. These are strong, proteinaceous fibres that mussels secrete to adhere themselves to rocks, preventing detachment by waves and predators. These byssal threads may be strengthened if mussels can recognize potential threats, such as native crabs, as their populations have a long history of coevolution. Unfortunately, the introduction of invasive predators poses a challenge for prey, which may not be capable of recognizing them. In this study, byssal thread production in the Pacific blue mussel (Mytilus trossulus ) was observed when exposed to effluent from the native red rock crab (Cancer productus) or the invasive European Green crab (Carcinus maenas). M. trossulus were placed in closed systems with effluent from either C. productus , C. maenas or control (no predator), over a 24-hour time period. Final measurements of number, length and diameter of byssal threads were recorded. M. trossulus exposed to effluent from C. productus produced byssal threads at a statistically significantly faster rate than in the control group over the first 7.5 hours. M. trossulus exposed to effluent from C. maenas produced byssal threads at a statistically significantly faster rate than both the C. productus and control groups. However, after 24 hours, there was no statistically significant difference between the mean number of byssal threads for any treatment. Additionally, we found no statistically significant difference between the mean diameter of byssal threads produced or length of byssal threads produced for any treatment.

Functional morphology ofCardiomya cleryana(d'Orbigny, 1842) (Bivalvia: Anomalodesmata: Cuspidariidae) from Brazilian waters: new insights into the lifestyle of carnivorous bivalves

Of the more than 800 Recent species of Anomalodesmata only 16 have been studied alive. The Septibranchia, comprising a number of carnivorous bivalve superfamilies, are no exception to this generalization and, until recently, no living member of this group has been studied since the 1980s. Collected from the shallow, shelf seabed off Brazil,Cardiomya cleryanais one of only a few species to have its morphology described in recent years and the first ever anomalodesmatan to be filmed alive. Important anatomical features such as a greatly extensible foot to secure itself in the sediment with a single byssal thread, exhalant siphon inter-tentacular projections and micro-papillae on the surface of the siphonal tentacles are described. Observations on the species’ behaviour have revealed a lifestyle hitherto not recorded for any septibranch, indeed any anomalodesmatan. The anchoring mechanism ofC. cleryanausing an extraordinarily long byssal thread is described for the first time. The life position ofC. cleryanais at 45° to the sediment-water interface whereas other cuspidariids have been considered to orient themselves vertically. An anatomical comparison betweenCardiomyaandBathyneaerahas revealed close affinities. This study thus provides new insights into the morphology and behaviour of the Cuspidariidae.

Functional morphology, biology and sexual strategy of the circumboreal, adventitious crypt-building,Crenella decussata(Bivalvia: Mytiloidea: Crenellidae)

The anatomy ofCrenella decussata(Mytiloidea) is described. Individuals of this circumboreal species occupy granular crypts composed of sand grains held in place by mucus. The swollen basal region of the tubule is occupied by an individual, which connects to the sediment surface by two posterior tubes accommodating the inhalant and exhalant streams. There is reduction in musculature and, most importantly, anterior foreshortening of the outer ctenidial demibranchs and loss of the labial palps. This creates an anterior space in the mantle for the initial brooding of fertilized ova by females to the prodissoconch stage. Subsequently, these larvae are transferred to the exhalant tube of the crypt wherein they attach by a single fine byssal thread and are further brooded until the crawl-away juvenile stage is attained. Experimental studies of larval behaviour suggest that parental pheromones sustain the female/offspring bond. Newly hatched individuals responded to parental exhalant water by actively attaching themselves using a byssal thread. This response persisted for 28 days, but not after 55 days when, we suggest, the pheromonal response ceases and offspring are developed sufficiently to take up life in their own nests. Offspring retrieved from parental crypts and fed continuously reached an average shell length of 500 μm after 7.5 months. Brooded offspring thus appear to rely on embryonal energy resources until post-metamorphosis, after which suspension feeding becomes essential for further growth and development before the parental crypt is vacated.

Mechanical homeostasis of a DOPA-enriched biological coating from mussels in response to metal variation

Protein–metal coordination interactions were recently found to function as crucial mechanical cross-links in certain biological materials. Mussels, for example, use Fe ions from the local environment coordinated to DOPA-rich proteins to stiffen the protective cuticle of their anchoring byssal attachment threads. Bioavailability of metal ions in ocean habitats varies significantly owing to natural and anthropogenic inputs on both short and geological spatio-temporal scales leading to large variations in byssal thread metal composition; however, it is not clear how or if this affects thread performance. Here, we demonstrate that in natural environments mussels can opportunistically replace Fe ions in the DOPA coordination complex with V and Al. In vitro removal of the native DOPA–metal complexes with ethylenediaminetetraacetic acid and replacement with either Fe or V does not lead to statistically significant changes in cuticle performance, indicating that each metal ion is equally sufficient as a DOPA cross-linking agent, able to account for nearly 85% of the stiffness and hardness of the material. Notably, replacement with Al ions also leads to full recovery of stiffness, but only 82% recovery of hardness. These findings have important implications for the adaptability of this biological material in a dynamically changing and unpredictable habitat.