Intertidal Mussel Research Articles

Unravelling the Brachidontes variabilis species complex (Bivalvia: Mytilidae) of the Indo-Pacific region

ABSTRACT Members of the radially ribbed mytilid genus Brachidontes are often dominant filter feeders on hard intertidal substrata in the Indo-Pacific region. However, there is still a great deal of uncertainty and confusion over their species identities, taxonomy and phylogenetic relationships. At least six species names (crebristriatus, karachiensis, mutabilis, pharaonis, ustulatus and variabilis) have at one time or another been synonymized with each other and applied to these common intertidal mussels. They occur widely across the Indian and Pacific Oceans from East Africa to Hawaii. Our results, based on sequences of five genes and anatomical features, suggest there are at least eight closely related sibling species in three monophyletic clades: (1) Brachidontes variabilis-form A in the western Indian Ocean; (2) Brachidontes pharaonis in the Red Sea; (3) Brachidontes variabilis-form B, found from India to East Asia; (4) Brachidontes mutabilis, restricted to southern Japan and China; (5) Brachidontes crebristriatus, in the Indian Ocean through to Southeast Asia and Hawaii; (6) Brachidontes ustulatus, an endemic species in western and southern Australia; (7) Brachidontes maritimus, so far known only from Hawaii; and (8) Brachidontes erosus, a southern Australian endemic. The latter two species form a small clade (Clade 1) that is sister to two larger Clades 2 and 3, each comprising three species. Clade 2 contains Brachidontes crebristriatus, Brachidontes mutabilis and Brachidontes ustulatus, whilst Clade 3 is made up of Brachidontes pharaonis, Brachidontes variabilis-form A and variabilis-form B. The shells of these eight species are not only variable but can greatly overlap in morphology. Many are also nearly impossible to distinguish without geographical information. However, the absence or presence of plicate organs in the mantle cavity, and the shape of guard papillae lining the inhalant aperture, may serve as important diagnostic morphological characters when used alongside geographical provenance.

Changes in the composition of invertebrate assemblages from wave-exposed intertidal mussel stands along the Nova Scotia coast, Canada.

Rocky intertidal habitats occur worldwide and are mainly characterized by primary space holders such as seaweeds and sessile invertebrates. Some of these organisms are foundation species, as they can form structurally complex stands that host many small invertebrates. The abundance of primary space holders is known to vary along coastlines driven directly or indirectly by environmental variation. However, it is less clear if the invertebrate assemblages associated to a foundation species may remain relatively unchanged along coastlines, as similar stands of a foundation species can generate similar microclimates. We examined this question using abundance data for invertebrate species found in mussel stands of a similar structure in wave-exposed rocky habitats at mid-intertidal elevations along the Atlantic coast of Nova Scotia (Canada). While the most abundant invertebrate species were found at three locations spanning 315 km of coastline, species composition (a combined measure of species identity and their relative abundance) differed significantly among the locations. One of the species explaining the highest amount of variation among locations (a barnacle) exhibited potential signs of bottom-up regulation involving pelagic food supply, suggesting benthic-pelagic coupling. The abundance of the species that explained the highest amount of variation (an oligochaete) was positively related to the abundance of their predators (mites), further suggesting bottom-up forcing in these communities. Overall, we conclude that species assemblages associated to structurally similar stands of a foundation species can show clear changes in species composition at a regional scale.

Variations in the heart rate of Mediterranean mussels Mytilus galloprovincialis and brown mussels Perna perna under thermal stress on rocky shores of South Africa

Intertidal mussels experience prolonged emersion during low tide, followed by rapid submergence cooling during high tide, causing temperature-induced stress responses. This study examined variations in heart rate to investigate the relationship between emerged and submerged thermal stress in Mediterranean mussels Mytilus galloprovincialis and brown mussels Perna perna from one site on a south coast warm-water coastline and two sites on a west coast cold-water coastline in South Africa. Gaping behaviour in air displayed by P. perna appears to contribute towards their survivability under warmer conditions, as their flatline temperature was higher as compared with M. galloprovincialis, which do not display gaping behaviour. Warm-water acclimatised mussels of both species appeared better able to survive higher temperatures than cold-water acclimatised mussels. However, both mussel species are possibly living at their upper thermal tolerance based on their sublethal Arrhenius breakpoint temperature (ABT). The values of ABT were higher while exposed to air than when submerged, revealing physiological mechanisms at work to cope with changes in the intertidal zone.

Interpreting life-history traits, seasonal cycles, and coastal climate from an intertidal mussel species: Insights from 9000 years of synthesized stable isotope data.

Understanding past coastal variability is valuable for contextualizing modern changes in coastal settings, yet existing Holocene paleoceanographic records for the North American Pacific Coast commonly originate from offshore marine sediments and may not represent the dynamic coastal environment. A potential archive of eastern Pacific Coast environmental variability is the intertidal mussel species Mytilus californianus. Archaeologists have collected copious stable isotopic (δ18O and δ13C) data from M. californianus shells to study human history at California's Channel Islands. When analyzed together, these isotopic data provide windows into 9000 years of Holocene isotopic variability and M. californianus life history. Here we synthesize over 6000 δ18O and δ13C data points from 13 published studies to investigate M. californianus shell isotopic variability across ontogenetic, geographic, seasonal, and millennial scales. Our analyses show that M. californianus may grow and record environmental information more irregularly than expected due to the competing influences of calcification, ontogeny, metabolism, and habitat. Stable isotope profiles with five or more subsamples per shell recorded environmental information ranging from seasonal to millennial scales, depending on the number of shells analyzed and the resolution of isotopic subsampling. Individual shell profiles contained seasonal cycles and an accurate inferred annual temperature range of ~ 5°C, although ontogenetic growth reduction obscured seasonal signals as organisms aged. Collectively, the mussel shell record reflected millennial-scale climate variability and an overall 0.52‰ depletion in δ18Oshell from 8800 BP to the present. The archive also revealed local-scale oceanographic variability in the form of a warmer coastal mainland δ18Oshell signal (-0.32‰) compared to a cooler offshore islands δ18Oshell signal (0.33‰). While M. californianus is a promising coastal archive, we emphasize the need for high-resolution subsampling from multiple individuals to disentangle impacts of calcification, metabolism, ontogeny, and habitat and more accurately infer environmental and biological patterns recorded by an intertidal species.

Drone-based monitoring of intertidal blue mussel beds in the Wadden Sea – comparison of a threshold and two machine learning approaches

In the Wadden Sea, intertidal mussel beds of the blue mussel (Mytilus edulis) and the Pacific oyster (Magallana gigas) form distinct epibenthic communities and local hotspots of high biomass and biodiversity. To detect and evaluate natural and anthropogenic processes, a ground-based monitoring program started over 25 years ago in the German Wadden Sea. In this study, we describe the potential of drones and machine learning approaches for a remote sensing-based integration into an existing monitoring program of intertidal mussel beds. A fixed wing drone was used to cover an area of up to 39ha in a single flight, with an overall time saving potential of 50%. Applying machine learning approaches, a detailed extraction of the intertidal blue mussel bed coverage with an overall accuracy (OA) up to 95.6% was reached, applying a Support Vector Machine (SVM). The application of a multispectral sensor improved the classification performance. Compared to ground-based monitoring, the drone-based method provided significantly more information on the area extension, coverage, and associated algae of the mussel beds. The results show that drones can provide a non-invasive way to survey large and difficult to access areas providing detailed maps of mussel beds and their internal structures.

Coastal topography and rates of mussel recruitment: a comparison of bay versus open-coast sites

The recruitment of intertidal benthic organisms that have planktonic larvae is influenced by hydrodynamics at multiple nested spatial scales, ranging from tens of centimetres to kilometres. Intertidal mussel populations on the south coast of South Africa are known to exhibit higher cover within bays than on open-coast shorelines. This study tested the hypothesis that topographically driven differences in hydrodynamics will result in comparatively higher recruitment within bays. Specifically, we estimated recruitment rates of the native brown mussel Perna perna and the invasive Mediterranean mussel Mytilus galloprovincialis (family Mytilidae) over five spring tidal cycles at bay and open-coast sites at both Algoa Bay and St Francis Bay, and the data were then correlated with upwelling indices derived from wind data. We recorded 3 313 P. perna and 2 485 M. galloprovincialis recruits individually and found that mussel recruitment within bays was as much as two orders of magnitude higher than on open coast. The relationship between recruit numbers and upwelling indices was positive, although non-significant, and markedly stronger for the open-coast sites (where r 2 values were 0.51–0.59). These results indicate that better mussel cover within bays can be at least partially explained by higher recruitment rates.

Non-native barnacle accelerates the recovery from disturbance of intertidal mussel beds

The barnacle Balanus glandula is a non-native species inhabiting Argentinian rocky shores. The native mussel Brachidontes rodriguezii forms extensive beds in the mid-intertidal zone of these shores, generating a physical structure that determines the diversity of the assemblage. Yet, this native foundation species is prone to mortality due to disturbances associated with extreme climatic events. The aim of this study was to experimentally investigate the role of early-colonizing, non-native B. glandula in the succession process and the recovery of mussel beds following disturbance. Experimental plots were demarcated in the mussel bed and initially cleared of mussels, to produce exposed rock surfaces similar to those that form after a disturbance event. Half of these plots were kept barnacle-free throughout the experiment by removing all recruiting B. glandula, whereas all recruits were allowed to develop in the remaining plots. Our results showed that mussel cover at the end of the experiment was higher in the plots with barnacles. The plots with and without barnacles followed different successional trajectories, with increasing limpet densities and reduced cover of crustose algae in the presence of barnacles during early successional stages. The results indicate that the presence of B. glandula at the early stages of succession can alter successional dynamics and facilitate the recovery of mussel bed cover after disturbance events. More broadly, this study also shows that non-native species, although frequently considered a ‘nuisance’, can accelerate the recovery of foundation species that characterize entire communities and sustain the greatest share of their diversity.

Intertidal mussels as ecosystem engineers: maintenance of invertebrate assemblages amid intertidal stress gradients

Species that form complex biogenic structures may increase niche space for many others and are assumed to be paramount for whole‐assemblage stability and ecosystem functioning. Because they often ameliorate physical conditions, ecosystem engineering species are also predicted to become more important with environmental stress. Testing this hypothesis, however, has proven difficult because isolating facilitation effects along the entire stress gradient is challenging. Here we addressed motile invertebrate assemblages associated to the mid‐intertidal chthamalid barnacle cover at four rocky shores, either with (‘facilitated') or without (‘control') a secondary natural cover of small mussels (Mytilaster solisianus and Brachidontes darwinianus). Following a factorial balanced design, replicate samples were taken at three tidal heights in all sites, encompassing a clear gradient of thermal stress and desiccation potential along the vertical range of the mussel‐enriched zone. While observations on general abundance were mostly consistent with stress‐independent facilitation, results for richness, diversity and assemblage structure indicated overarching stress‐dependent responses. All these later three response variables steadily declined from the low to the high level in the control barnacle habitat but remained unaltered in the mussel‐facilitated habitat. Increased facilitation higher on the shore is mostly due to retention of stress‐vulnerable groups such as polychaetes, flatworms and large nematodes which virtually collapse in the higher control habitat, further indicating that mechanisms of mussel facilitation involve relief of environmental stress rather than protection from higher‐order consumers. Our results suggest that mussel ecosystem engineering was fully preserved during the summer season when sampling took place. Ongoing research simulating heat waves compatible to climate‐change scenarios will test whether mussel facilitation would hold over the coming decades.

Mussels (Mytilus spp.) in Svalbard contain microplastic particles in tissues: Implications for monitoring

We examined the presence of microplastics in blue mussels Mytilus spp. from the intertidal zone of western Spitsbergen in Arctic Svalbard. The optical microscopy technique detected a total of 148 microplastics, with the highest concentration per mussel being 24 particles. Microplastics were found in 84% of the examined mussels. The microplastics ranged in size from <0.5 mm to 5 mm and consisted of fibers (83%), fragments (13%), plates (3%), and spherules (1%). The micro-Raman spectroscopy technique revealed four different types of polymers: polyethylene (67%), nylon-12 (17%), low-density polyethylene (11%), and polypropylene (5%). Our research shows that Arctic coastal waters are polluted with microplastics notwithstanding their remoteness. These findings suggest that microplastic contamination may harm marine life and coastal ecosystems and require further research into long-term environmental effects. We also indicate that intertidal mussels may be beneficial for monitoring microplastics because they can be collected without involving diving.

Transient species driving ecosystem multifunctionality: Insights from competitive interactions between rocky intertidal mussels

Anthropogenic biodiversity loss poses a significant threat to ecosystem functioning worldwide. Numerically dominant and locally rare (i.e., transient) species are key components of biodiversity, but their contribution to multiple ecosystem functions (i.e., multifunctionality) has been seldomly assessed in marine ecosystems. To fill this gap, here we analyze the effects of a dominant and a transient species on ecosystem multifunctionality. In an observational study conducted along ca. 200 km of the southeastern Pacific coast, the purple mussel Perumytilus purpuratus numerically dominated the mid-intertidal and the dwarf mussel Semimytilus patagonicus exhibited low abundances but higher recruitment rates. In laboratory experiments, the relative abundances of both species were manipulated to simulate the replacement of P. purpuratus by S. patagonicus and five proxies for ecosystem functions—rates of clearance, oxygen consumption, total biodeposit, organic biodeposit, and excretion—were analyzed. This replacement had a positive, linear, and significant effect on the combined ecosystem functions, particularly oxygen consumption and excretion rates. Accordingly, S. patagonicus could well drive ecosystem functioning given favorable environmental conditions for its recovery from rarity. Our study highlights therefore the key role of transient species for ecosystem performance. Improving our understanding of these dynamics is crucial for effective ecosystem conservation, especially in the current scenario of biological extinctions and invasions.

Microplastic leachates inhibit small-scale self-organization in mussel beds

Self-organized spatial patterns are increasingly recognized for their contribution to ecosystem functioning. They can improve the ecosystem's ability to respond to perturbation and thus increase its resilience to environmental stress. Plastic pollution has now emerged as major threat to aquatic and terrestrial biota. Under laboratory conditions, we tested whether plastic leachates from pellets collected in the intertidal can impair small-scale, spatial self-organization and byssal threads production of intertidal mussels and whether the effect varied depending on where the pellets come from. Specifically, leachates originating from plastic pellets collected from relatively pristine and polluted areas respectively impaired and inhibited the ability of mussels to self-organize at small-scale and to produce byssal threads compared to control conditions (i.e., seawater without leaching solution). Limitations to natural self-organizing processes and threads formation may translate to a declined capacity of natural ecosystems to avoid tipping points and to a reduced restoration success of disturbed ecosystems.

Physiologically informed organismal climatologies reveal unexpected spatiotemporal trends in temperature.

Body temperature is universally recognized as a dominant driver of biological performance. Although the critical distinction between the temperature of an organism and its surrounding habitat has long been recognized, it remains common practice to assume that trends in air temperature-collected via remote sensing or weather stations-are diagnostic of trends in animal temperature and thus of spatiotemporal patterns of physiological stress and mortality risk. Here, by analysing long-term trends recorded by biomimetic temperature sensors designed to emulate intertidal mussel temperature across the US Pacific Coast, we show that trends in maximal organismal temperature ('organismal climatologies') during aerial exposure can differ substantially from those exhibited by co-located environmental data products. Specifically, using linear regression to compare maximal organismal and environmental (air temperature) climatologies, we show that not only are the magnitudes of body and air temperature markedly different, as expected, but so are their temporal trends at both local and biogeographic scales, with some sites showing significant decadal-scale increases in organismal temperature despite reductions in air temperature, or vice versa. The idiosyncratic relationship between the spatiotemporal patterns of organismal and air temperatures suggests that environmental climatology cannot be statistically corrected to serve as an accurate proxy for organismal climatology. Finally, using quantile regression, we show that spatiotemporal trends vary across the distribution of organismal temperature, with extremes shifting in different directions and at different rates than average metrics. Overall, our results highlight the importance of quantifying changes in the entire distribution of temperature to better predict biological performance and dispel the notion that raw or 'corrected' environmental (and specially air temperature) climatologies can be used to predict organismal temperature trends. Hence, despite their widespread coverage and availability, the severe limitations of environmental climatologies suggest that their role in conservation and management policy should be carefully considered.

Algal cover as a driver of diversity in communities associated with mussel assemblages across eastern Pacific ecoregions

AbstractResearch on intertidal mussel assemblages and associated communities has revealed that complexity and structure are influenced by environmental heterogeneity and local‐scale factors affecting recruitment. Research in situ in eastern and western Pacific intertidal ecosystems has suggested drivers of species diversity and community structure encompassing large geographic scales, however, there are major gaps in geographic coverage. Our aim is to fill some of these gaps by analyzing macrofaunal functional group diversity and effects of environmental factors on intertidal mussel communities from three distinct marine ecoregions in the southern and northern hemispheres. We identified the effects of algal cover and environmental heterogeneity on species richness and evenness, and we modeled factors effecting mussel layer complexity from assemblages in three marine ecoregions. We analyzed macrofaunal species diversity within one of the austral ecoregions based on the width of the coastal shelf. Species richness was highest in samples from the northern hemisphere while evenness was highest in samples from the southern hemisphere. Similarity in functional group structure for all communities sampled was ≤55% (Bray–Curtis dissimilarity) and ≤35% (Chao–Jaccard dissimilarity). Wave exposure had a significant effect on shell length and complexity of mussel matrices on rocky bench platforms. The presence of algal cover had a strong effect on species richness in mussel matrices regardless of complexity, while algal canopies had no effect on species evenness. Overall, this study provides significant new insight on the community complexity of mussel beds in parts of the world which have been poorly studied in this regard.

Further Loss of Intertidal Mussel Stands on the Nova Scotia Coast (Canada) after the Passage of Cyclone Lee

Intertidal mussel stands are common on temperate rocky seashores and host many small invertebrates, so they are important biodiversity reservoirs. Their integrity, however, is being increasingly affected by environmental extremes. An unusual cold snap in Nova Scotia (Canada) in February 2023 was followed by the mass disappearance of mussel stands at mid-to-high elevations in rocky intertidal habitats. The present article presents evidence of significant losses at middle intertidal elevations following the passage of cyclone Lee in September 2023, which created severe surf conditions. The increasing occurrence of successive environmental extremes might challenge the persistence of these important biological systems.

Multi-omics reveals largely distinct transcript- and protein-level responses to the environment in an intertidal mussel.

Organismal responses to stressful environments are influenced by numerous transcript- and protein-level mechanisms, and the relationships between expression changes at these levels are not always straightforward. Here, we used paired transcriptomic and proteomic datasets from two previous studies from gill of the California mussel, Mytilus californianus, to explore how simultaneous transcript and protein abundance patterns may diverge under different environmental scenarios. Field-acclimatized mussels were sampled from two disparate intertidal sites; individuals from one site were subjected to three further treatments (common garden, low-intertidal or high-intertidal outplant) that vary in temperature and feeding time. Assessing 1519 genes shared between the two datasets revealed that both transcript and protein expression patterns differentiated the treatments at a global level, despite numerous underlying discrepancies. There were far more instances of differential expression between treatments in transcript only (1451) or protein only (226) than of the two levels shifting expression concordantly (68 instances). Upregulated expression of cilium-associated transcripts (likely related to feeding) was associated with relatively benign field treatments. In the most stressful treatment, transcripts, but not proteins, for several molecular chaperones (including heat shock proteins and endoplasmic reticulum chaperones) were more abundant, consistent with a threshold model for induction of translation of constitutively available mRNAs. Overall, these results suggest that the relative importance of transcript- and protein-level regulation (translation and/or turnover) differs among cellular functions and across specific microhabitats or environmental contexts. Furthermore, the degree of concordance between transcript and protein expression can vary across benign versus acutely stressful environmental conditions.

Metabolic scaling variation as a constitutive adaptation to tide level in Mytilus galloprovincialis

Understanding how allometric exponents vary in the different biologically determined patterns turns out to be fundamental for the development of a unifying hypothesis that intends to explain most of the variation among taxa and physiological states. The aims of this study were (i) to analyze the scaling exponents of oxygen consumption at different metabolic rates in Mytilus galloprovincialis according to different seasons, habitat, and acclimation to laboratory conditions and (ii) to examine the variation in shell morphology depending on habitat or seasonal environmental hazards. The allometric exponent for standard metabolic rate (b value) did not vary across seasons or tide level, presenting a consistent value of 0.644. However, the mass-specific standard oxygen consumption (a value), i.e. metabolic level, was lower in intertidal mussels (subtidal mussels: a = - 1.364; intertidal mussels: a = - 1.634). The allometric exponent for routine metabolic rate changed significantly with tide level: lower allometric exponents for intertidal mussels (b = 0.673) than for subtidal mussels (b = 0.871). This differential response did not change for at least two months after the environmental cue was removed. We suggest that this is the result of intertidal mussels investing fundamentally in surface-dependent organs (gill and shell), with the exception of the slightly higher values obtained in May as a likely consequence of gonadal tissue development. Subtidal mussels, on the contrary, are probably in constant demand for volume-related resources, which makes them consistently obtain an allometric exponent of around 0.87.

Identifying how restoration measures influence the presence of shorebirds: a case study on the use of artificial structures for restoring mussel reefs

Artificial structures are often used as a tool for habitat restoration and the recreation of degraded coastal ecosystems and their associated food webs. However, it is often unknown if and how these artificial structures may influence the habitat use of target species, thereby hampering restoration goals. In this study, we test how artificial barriers, deployed to enhance the creation of an intertidal mussel bed, influenced the mussel‐habitat use by two bird species under pressure, Eurasian oystercatchers and Eurasian curlews. Average bird presence was monitored using time‐lapse camera's from the start of the mussel bed restoration in August 2018 until April 2019. We found that in the first few months of the experiment, both oystercatchers and curlews avoided the restored mussel beds containing artificial structures in the form of metal barriers that act as traps for dislodged mussels. Thereafter, the presence of barriers had no negative influence on the average presence of oystercatchers or curlews. In fact, curlews were significantly attracted to the mussel beds with barriers in January and February. In addition, we found a negative effect of the presence of European herring gulls on the presence of oystercatchers and curlews. The higher herring gull densities in the first 2 months of the experiment might explain the lower‐than‐expected curlew and oystercatcher densities observed in August. To our knowledge, no other studies have investigated the effect of artificial restoration structures on the abundance or habitat use of specific shorebirds.

The impacts of thermal heterogeneity across microhabitats on post-settlement selection of intertidal mussels

Rapid genetic selection is critical for allowing natural populations to adapt to different thermal environments such as those that occur across intertidal microhabitats with high degrees of thermal heterogeneity. To address the question of how thermal regimes influence selection and adaptation in the intertidal black mussel Mytilisepta virgata, we continuously recorded environmental temperatures in both tidal pools and emergent rock microhabitats and then assessed genetic differentiation, gene expression patterns, RNA editing level, and cardiac performance. Our results showed that the subpopulations in the tidal pool and on emergent rocks had different genetic structures and exhibited different physiological and molecular responses to high-temperature stress. These results indicate that environmental heterogeneity across microhabitats is important for driving genetic differentiation and shed light on the importance of post-settlement selection for adaptively modifying the genetic composition and thermal responses of these intertidal mussels.

Mass disappearance of intertidal mussels after an unusual winter cold snap in eastern Canada.

Mass disappearance of intertidal mussels after an unusual winter cold snap in eastern Canada.

Intraspecific variation in a predator changes intertidal community through effects on a foundation species.

Intraspecific variation is an important form of biodiversity that can alter community and ecosystem properties. Recent work demonstrates the community effects of intraspecific variation in predators via altering prey communities and in foundation species via shaping habitat attributes. However, tests of the community effects of intraspecific trait variation in predators acting on foundation species are lacking despite the fact that consumption of foundation species can have strong community effects by shaping habitat structure. Here, we tested the hypothesis that intraspecific foraging differences among populations of mussel-drilling dogwhelk predators (Nucella) differentially alter intertidal communities through effects on foundational mussels. We conducted a 9-month field experiment where we exposed intertidal mussel bed communities to predation from three Nucella populations that exhibit differences in size-selectivity and consumption time for mussel prey. At the end of the experiment, we measured mussel bed structure, species diversity, and community composition. While exposure to Nucella originating from different populations did not significantly alter overall community diversity, we found that differences in Nucella mussel selectivity significantly altered foundational mussel bed structure, which in turn altered the biomass of shore crabs and periwinkle snails. Our study extends the emerging paradigm of the ecological importance of intraspecific variation to include the effects of intraspecific variation on predators of foundation species.