Intertidal Mussel Mytilus Californianus Research Articles

Elevated aerial temperature modulates digestive enzyme activities in Mytilus californianus.

The marine intertidal mussel Mytilus californianus aggregates to form beds along the Pacific shores of North America. As a sessile organism it must cope with fluctuations in temperature during low-tide aerial exposure, which elevates maintenance costs and negatively affects its overall energy budget. The function of its digestive gland is to release enzymes that break apart ingested polymers for subsequent nutrient absorption. The effects of elevated aerial warming acclimation on the functioning of digestive gland enzymes are not well studied. In this study we asked whether digestive gland carbohydases and proteases could be overstimulated in warm condition to possibly mitigate the costs related to the heat-shock response. We compared mussels acclimated to a+9°C heat-shock during daily low-tide aerial exposure to mussels acclimated to isothermal tidal conditions in a simulated intertidal system. The results showed fairly consistent activities of cellulase, trypsin, and amino-peptidase across tidal variation and between thermal treatments; however, amylase activity was lower in warmed versus cool mussels across low and high-tide. We also observed the expression of heat-shock genes in gill tissue during warm tidal conditions, suggestive that moderate temperatures during aerial exposure can induce a stress response.

Bivalves rapidly repair shells damaged by fatigue and bolster strength.

ABSTRACTHard external armors have to defend against a lifetime of threats yet are traditionally understood by their ability to withstand a single attack. Survival of bivalve mollusks thus can depend on the ability to repair shell damage between encounters. We studied the capacity for repair in the intertidal mussel Mytilus californianus by compressing live mussels for 15 cycles at ∼79% of their predicted strength (critically fracturing 46% of shells), then allowing the survivors 0, 1, 2 or 4 weeks to repair. Immediately after fatigue loading, mussel shells were 20% weaker than control shells that had not experienced repetitive loading. However, mussels restored full shell strength within 1 week, and after 4 weeks shells that had experienced greater fatiguing forces were stronger than those repetitively loaded at lower forces. Microscopy supported the hypothesis that crack propagation is a mechanism of fatigue-caused weakening. However, the mechanism of repair was only partially explained, as epifluorescence microscopy of calcein staining for shell deposition showed that only half of the mussels that experienced repetitive loading had initiated direct repair via shell growth around fractures. Our findings document repair weeks to months faster than demonstrated in other mollusks. This rapid repair may be important for the mussels’ success contending with predatory and environmental threats in the harsh environment of wave-swept rocky coasts, allowing them to address non-critical but weakening damage and to initiate plastic changes to shell strength. We highlight the significant insight gained by studying biological armors not as static structures but, instead, as dynamic systems that accumulate, repair and respond to damage.

Circadian and circatidal rhythms of protein abundance in the California mussel (Mytilus californianus).

Coastal habitats fluctuate with the 12.4h tidal and 24h light/dark cycle to predictably alter conditions such as air exposure, temperature, and food availability. Intertidal sessile bivalves exhibit behavioural and physiological adjustments to minimize the challenges of this environment. We investigated a high-resolution time course of the changes in protein abundance in the gill tissue of the intertidal mussel Mytilus californianus in a simulated tidal environment of 12:12h light:dark cycles and a matching 6:6h high:low tide cycle within each 12h period. Approximately 38% of detected proteins showed significant rhythms in their abundances, with diversity in the phases of rhythmic isoforms. The circadian rhythm was dominant in protein abundance changes, particularly with oxidative metabolism. A tidal cycle elicited changes within functional groups, including in cytoskeletal proteins, chaperones, and oxidative stress proteins. In addition to protein abundance changes, we found the possibility for post-translational modifications driving rhythms, including methylation, mitochondrial peptide processing (proteolysis), and acylation. Dynamic changes in the proteome across functional categories demonstrate the importance of the tidal environment in entraining cellular processes, confirming that differential expression studies should not assume a static baseline of cellular conditions in intertidal organisms.

Cycles of heat and aerial-exposure induce changes in the transcriptome related to cell regulation and metabolism in Mytilus californianus

The intertidal mussel Mytilus californianus is subjected to thermal and oxygen cycles due to fluctuations of the tidal cycle. Mussels that reside in high-shore microenvironments experience extended periods of aerial-exposure and greater thermal challenges than low-shore populations. In this study, we investigated the combined effect of daily extended periods of aerial-exposure and midday thermal events on the physiology of mussels by monitoring transcriptome-wide gene expression in a simulated tidal environment. Mussels were acclimated to aerial-exposure for 20 h a day combined with a simulated midday solar heating event of + 8 °C. Results revealed that 11% of the transcriptome exhibited robust patterns of rhythmic gene expression. Two broad sets of genes were induced, including one that was upregulated during the daytime thermal stress period and another following the 4-h evening high-tide. The daytime thermal stress associated gene set was enriched for genes related to cellular regulatory pathways such as those that encode transcription factors while genes expressed following evening submergence varied in functional theme. Additionally, genes related to energy metabolism were also upregulated during warming periods of the tidal cycle. Comparing these data to published data from a previous tidal simulation study revealed that acclimation to daily heat stress yielded a muted transcriptional response to heat compared to an acute response observed in mussels maintained under isothermal conditions. These results indicate that M. californianus displays phenotypic plasticity with respect to transcriptomic expression and that this trait likely promotes homeostasis in the intertidal environment.

Inter-individual physiological variation in responses to environmental variation and environmental change: Integrating across traits and time

Greater understanding of physiological responses to climate change demands deeper comprehension of the causes and consequences of physiological variation. Increasingly, population trait means are being deconstructed into variable signals at the level of individuals. We advocate for greater consideration of such inter-individual physiological variation and how it both depends on and interacts with environmental variability. First, we review several studies on the intertidal mussel Mytilus californianus to illustrate how the magnitude of inter-individual variation may depend on the environmental context analyzed (i.e., is the mean condition benign or stressful?) and/or on the specific physiological metric investigated. Stressful conditions may reveal or mask variation in disparate ways at different levels of analysis (e.g., transcriptome vs. proteome), but we often lack crucial information regarding the relationships among these different physiological metrics and their consequences for fitness. We then reanalyze several published datasets to ask whether individuals employ divergent strategies over time in response to acute heat stress; such time-dependence would further complicate interpretation of physiological variation. However, definitive conclusions are precluded by limited sample sizes and short timescales in extant datasets. A key remaining challenge is to extend these analytical frameworks to longer periods over which individuals in a population experience repeated, but spatially variable, episodic stress events. We conclude that variation at multiple levels of analysis should be investigated over longer periods and, where possible, within individuals (or genotypes) experiencing repeated environmental challenges. Although difficult in practice, such studies will facilitate improved understanding of potential population-level physiological responses to climate change.

Compressive strength of Mytilus californianus shell is time-dependent and can influence the potential foraging strategies of predators

The calcareous exoskeletons of bivalve molluscs protect the organisms from environmental stressors, including physical loads like impacts (e.g., from wave-borne rocks) and compressions (e.g., from predators). The magnitude and time scales of physical loads can occur over a wide range of values, and little is known about how the strength of bivalve shells are affected by the speed of impact or compression. We used the intertidal mussel Mytilus californianus to test how the rate of compression affects the strength of the mussel’s shell. Shell strength was time-dependent, and shells withstood 11.5% larger loads if those loads were applied quickly than if they were applied slowly. We then tested whether the shell’s time-dependent strength could influence the strategy of predators trying to compress and fracture the shells. Between strategies with the same compression rate, using more force reduced the time and mechanical work to fracture shells. However, between strategies with the same force, compressing shells slowly reduced the time required to fracture large shells, while the opposite was true for small shells. These results indicate that shell strength is not a static property. Time-dependent strength can influence the interactions between mussels and the physical loads they experience in nature, including their interactions with predators. Studies investigating the influence of climate change on the architecture and strength of mollusc shells should incorporate a range of ecologically relevant compression rates in their measurements to better understand how climate change will affect these organisms.

Modulation of digestive physiology and biochemistry in Mytilus californianus in response to feeding level acclimation and microhabitat.

ABSTRACTThe intertidal mussel Mytilus californianus is a critical foundation species that is exposed to fluctuations in the environment along tidal- and wave-exposure gradients. We investigated feeding and digestion in mussels under laboratory conditions and across environmental gradients in the field. We assessed whether mussels adopt a rate-maximization (higher ingestion and lower assimilation) or a yield-maximization acquisition (lower ingestion and higher assimilation) strategy under laboratory conditions by measuring feeding physiology and digestive enzyme activities. We used digestive enzyme activity to define resource acquisition strategies in laboratory studies, then measured digestive enzyme activities in three microhabitats at the extreme ends of the tidal- and wave-exposure gradients within a stretch of shore (<20 m) projected sea-ward. Our laboratory results indicated that mussels benefit from a high assimilation efficiency when food concentration is low and have a low assimilation efficiency when food concentration is high. Additionally, enzyme activities of carbohydrases amylase, laminarinase and cellulase were elevated when food concentration was high. The protease trypsin, however, did not increase with increasing food concentration. In field conditions, low-shore mussels surprisingly did not have high enzyme activities. Rather, high-shore mussels exhibited higher cellulase activities than low-shore mussels. Similarly, trypsin activity in the high-shore-wave-sheltered microhabitat was higher than that in high-shore-wave-exposed. As expected, mussels experienced increasing thermal stress as a function of reduced submergence from low to high shore and shelter from wave-splash. Our findings suggest that mussels compensate for limited feeding opportunities and thermal stress by modulating digestive enzyme activities.

Predicting intertidal organism temperatures with modified land surface models

Animals and plants in the marine intertidal zone live at the interface between terrestrial and marine environments. This zone is likely to be a sensitive indicator of the effects of climate change in coastal ecosystems, because of several key characteristics including steep environmental gradients, rapid temperature changes during tide transitions, fierce competition for limited space, and a community of mostly sessile organisms. Here we describe a modular modeling approach using modifications to a meteorological land surface model to determine body temperatures of the ecologically dominant rocky intertidal mussel Mytilus californianus, as a tool that can be used as a proxy for ecological performance. We validate model results against in situ measurements made with biomimetic body temperature sensors. Model predictions lie within the range of variability of biomimetic measurements, based on observations over a 4-year period at sites along 1700 km of the US west coast from southern California (34.5°N) to northern Washington (48.4°N). Our modular approach can be easily applied to many situations in the intertidal zone, including bare rock, mussel, barnacle, and algal beds, salt-marsh grasses, and sand- and mud-flats, by modifying the “vegetation layer” in a standard meteorological land surface model. Biophysical models such as these, which link ecological processes to changing climates through predictions of body temperature, are essential for understanding biogeographic patterns of physiological stress and mortality risk.

INTERTIDAL MUSSELS EXHIBIT ENERGETIC TRADE-OFFS BETWEEN REPRODUCTION AND STRESS RESISTANCE

Life-history theory suggests that trade-offs exist between fitness components, with organisms balancing investment in reproduction against survival and future reproduction. This study examined the influence of stress on physiological trade-offs in the dominant rocky intertidal mussel Mytilus californianus on the central Oregon coast, USA. The intertidal zone is a highly heterogeneous thermal environment that could lead to intrapopulation variation in stress responses. Stress increases along a vertical gradient, with higher physical stress occurring in the higher intertidal zone, both due to reduced feeding time and longer exposure to aerial conditions. Reproduction and carotenoid content were compared in mussels from the low and high vertical edges of the mussel bed. High-edge mussels invested less relative energy in reproduction and also spawned all of their gametes in the early summer, whereas low-edge mussels continuously spawned small batches of gametes throughout the year. High-edge mussels accumulated high concentrations of carotenoid pigments into their gonadal tissues, potentially to protect gametes from damaging oxidative stress experienced during aerial exposure. A reciprocal transplant experiment revealed plastic responses in growth and reproduction to increased stress. In contrast, carotenoid content did not increase in response to stress, suggesting that carotenoids may not change rapidly or may not be easily lost or gained. Our results indicate that mussels exhibit physiological trade-offs and, under increased stress predicted from climate change scenarios, may allocate energy away from reproduction toward costly physiological defenses.

Gene expression in the intertidal mussel Mytilus californianus: physiological response to environmental factors on a biogeographic scale

MEPS Marine Ecology Progress Series Contact the journal Facebook Twitter RSS Mailing List Subscribe to our mailing list via Mailchimp HomeLatest VolumeAbout the JournalEditorsTheme Sections MEPS 356:1-14 (2008) - DOI: https://doi.org/10.3354/meps07354 Gene expression in the intertidal mussel Mytilus californianus: physiological response to environmental factors on a biogeographic scale Sean P. Place, Michael J. O’Donnell, Gretchen E. Hofmann* Department of Ecology, Evolution and Marine Biology, University of California Santa Barbara, Santa Barbara, California 93106-9610, USA *Corresponding author. Email: hofmann@lifesci.ucsb.edu ABSTRACT: We used a cDNA microarray to profile gene expression in the intertidal mussel Mytilus californianus across major portions of its biogeographic range. Overall, the expression pattern for the majority of genes assessed in this study varied significantly as a function of collection site and provides support for the hypothesis that the physiological response to emersion is distinct across populations of M. californianus. Gill tissue was dissected from adult, field-acclimatized M. californianus collected from 4 sites across 17° of latitude along the west coast of North America. First-strand cDNA prepared from 5 biological replicates from each site were competitively hybridized to a 2496 feature cDNA microarray. Gene expression patterns in mussels from Strawberry Hill, Oregon, displayed a unique expression phenotype that was distinct from the other 3 mussel populations sampled. In contrast, mussels sampled from Bamfield, British Columbia, and Jalama Beach, California, showed similar expression patterns. These data suggest that the physiological response of M. californianus to abiotic factors, such as temperature, cannot be predicted by a simple latitudinal gradient. This study highlights the usefulness of genomics-based approaches in assessing physiological responses to environmental variation across large spatial scales. KEY WORDS: Environmental genomics · Mytilus californianus · DNA microarray · Biogeography · Gene expression · Species range · Intertidal invertebrates · Mussel Full text in pdf format NextCite this article as: Place SP, O’Donnell MJ, Hofmann GE (2008) Gene expression in the intertidal mussel Mytilus californianus: physiological response to environmental factors on a biogeographic scale. Mar Ecol Prog Ser 356:1-14. https://doi.org/10.3354/meps07354 Export citation RSS - Facebook - Tweet - linkedIn Cited by Published in MEPS Vol. 356. Online publication date: March 18, 2008 Print ISSN: 0171-8630; Online ISSN: 1616-1599 Copyright © 2008 Inter-Research.

Complex patterns of expression of heat‐shock protein 70 across the southern biogeographical ranges of the intertidal mussel Mytilus californianus and snail Nucella ostrina

AbstractAim It is often assumed that species reach their highest densities in the centre of their ranges and decline in abundance toward the edges of the range. Implicit in this notion, which we call the abundant centre hypothesis, is the assumption that the edges of the range are more stressful to organisms and are more likely to show responses to climate change. However, an earlier review and empirical study of patterns of abundance across the range of intertidal invertebrates show little support for the abundant centre hypothesis and further demonstrated that few studies have examined patterns in either abundance or stress across species ranges. In part this gap is due to the logistical difficulties of sampling species across large geographical ranges. Here we use intertidal invertebrates, which have relatively simple linear latitudinal ranges, and heat‐shock proteins, which have been shown to be an integrative measure of organismal stress, to test the hypothesis that species are more stressed at the edges of their range. We use complementary data on population density to test the relationship between stress proteins and overall species density across the species’ range.Location Our sampling programme covered the southern half of the large geographical ranges of two intertidal invertebrates on the Pacific Coast of North America. Sites were spread between northern Baja California, Mexico and Vancouver Island, Canada, a range of c. 22 degrees of latitude.Method We sampled levels of heat‐shock protein 70 (Hsp70) in eight to 12 individuals from each of 20 sites for the intertidal mussel Mytilus californianus and 11 sites for the intertidal snail Nucella ostrina, spread throughout the southern half of their geographical ranges. The relationships between levels of Hsp70 in individuals from a site and (1) latitude of the site, (2) the site's position in the species’ range and (3) average population density were determined.Results No significant relationship was found in either species between levels of Hsp70 and latitude, position in the range or population density. Complex patterns that did emerge may be explained by nonlinear gradients in environmental conditions along the Pacific coast. Specifically, we observed peak values of Hsp70 for both species in northern Oregon, where intertidal zones are disproportionately exposed to daytime emersion (exposure to air) in the summer months of collections. A second peak for M. californianus was found south of Point Conception, California, which is marked by dramatic shifts toward warmer sea temperatures and decreased wave exposure.Main conclusions Patterns that emerged were not predicted by simple models based on the abundant centre hypothesis. However, they are consistent with more complex pictures of heat stress, organismal condition and abundance along a latitudinal gradient that have been demonstrated in recent studies. We suggest that latitudinal complexity, species‐specific differences and local effects must be considered before generalizing the relationship between environmental stress, abundance, range limits and responses of ranges to climate change.

Testing the effects of wave exposure, site, and behavior on intertidal mussel body temperatures: applications and limits of temperature logger design

The rocky intertidal mussel Mytilus californianus is exposed to potentially damaging thermal conditions during low tide. However, because the temperatures of ectothermic organisms are driven by multiple climatic factors, we do not fully understand what the body temperatures of intertidal invertebrates are under field conditions, or how thermal stress varies between intertidal sites. We designed a temperature logger that thermally matches (similar size, color, morphology and thermal inertia) living mussels of the species M. californianus, and tested its ability to provide realistic measurements of body temperature in the field. As part of these tests, we examined the propensity of M. californianus to “gape,” a behavior in which the mussel opens its shell valves, and which may permit evaporative cooling. Because our instruments were unable to mimic this behavior, we tested the degree to which gaping contributes to animal cooling by exposing M. californianus to a range of climatic conditions while recording body temperatures, gaping behavior and water loss. Results indicated no significant influence of gaping on body temperature. Tests comparing temperatures of loggers to those of real mussels under laboratory and field conditions showed that thermally matched loggers recorded temperatures within a few degrees of living animals and that unmodified loggers regularly incurred errors of up to 14°C. We then deployed a series of thermally matched loggers at two sites in central Oregon (Boiler Bay and Strawberry Hill) previously hypothesized to display site-specific differences in aerial temperature, and at various wave-exposure regimes within each site. Significant differences were demonstrated between sites using a subset of temperature metrics in a multivariate analysis. Yearly peaks in maximum temperature, average daily maximum temperature, and degree hours were useful in discriminating between sites. In 2001, wave-exposed sites at Strawberry Hill displayed fewer degree–hours than wave-protected sites, but an equivalent or greater maximum temperature. In 2002 both of these metrics were significantly lower in wave-exposed sites. Boiler Bay and Strawberry Hill differed in thermal regime, but not in a way that would indicate one was “hotter” than the other.

Local selection and latitudinal variation in a marine predator-prey interaction.

Although pairs of species often interact over broad geographic ranges, few studies have explored how interactions vary across these large spatial scales. Surveys along 1500 kilometers of the Pacific coast of North America documented marked variation in the frequency of predation by the snail Nucella canaliculata on the intertidal mussel Mytilus californianus. Laboratory rearing experiments suggest that regional differences in drilling behavior have a genetic basis, and mitochondrial sequence variation confirms that gene flow is low among these snail populations. Marine communities separated by hundreds of kilometers may have intrinsically different dynamics, with interactions shaped by restricted gene flow and spatially varying selection.

Marine oil pollution index

A Marine Oil Pollution Index (MOPI) is presented to characterize the hydrocarbon burdens of marine tissues or sediments. The index incorporates the ratios of unresolved to resolved components, even n -alkanes to odd n -alkanes, and branched hydrocarbons to n -alkanes, plus the total recoverable aliphatic and aromatic hydrocarbon concentrations from gas chromatographic analysis, to yield a single value that can be used to compare the relative magnitude of oil contamination in a series of tissue or sediment samples. Several examples of tissue samples from the intertidal mussel Mytilus californianus are presented, along with results from the 1975-78 BLM Southern California Baseline Study and MMS-sponsored Georges Bank Monitoring Program, to demonstrate the usefulness of generating single index values for time-series or spatial trend analyses. MOPI values calculated for analyzed tissue samples reflect varying degrees of exposure, ranging from pristine to heavily petrogenic conditions. A MOPI value calculated for a drilling fluid sample containing diesel oil residues also reflects the heavily petrogenic contamination.

Mercury in tissues of mussel off southern California

Total mercury content has been determined in three tissues of the intertidal mussel Mytilus californianus collected at locations along the southern California coast and at island control stations. The apparent influence of certain harbours and municipal wastewater outfalls was reflected by the relatively higher levels of mercury in all tissues of mussels from these areas. In general, the concentrations reported here are lower than those in mussels on west European coasts.

Trace metals in southern Californian mussels

The intertidal mussel Mytilus californianus is a useful indicator of anthropogenic inputs of several trace metals off southern California. Highest metal concentrations were measured in the digestive glands, and no significant differences attibutable to sex were found for this tissue. The distribution of lead appears to be dominated by diffuse inputs, while those of copper, chromium, and silver are most related to urban point sources. No distinct pattern was observed for nickel or zinc.