Posts Tagged 'performance'

Otolith development and elemental incorporation in response to seawater acidification in the flounder Paralichthys olivaceus at early life stages


  • Ocean acidification promoted otolith growth but not changed otolith shape.
  • Ocean acidification did not alter somatic growth or otolith elemental incorporation.
  • Ocean acidification induced and increased the occurrence of irregular calcitic otoliths.
  • Elemental incorporation is higher in aragonitic otoliths than in calcitic otoliths.


Ocean acidification can influence the formation, development and functions of calcified structures in marine organisms, such as otoliths, which are mainly composed of calcium carbonate (CaCO3) and function in orientation, balance, sensory perception and locomotion in fish. This study investigated the impacts of seawater acidification (pH 8.10, 7.70 and 7.30, roughly corresponding to the ocean acidification under RCP 8.5 scenario predicted by the IPCC) on somatic growth, otolith (aragonite) morphology and microchemistry in the flounder Paralichthys olivaceus at early life stages (ELSs, exposed to acidified seawater via pCO2 from embryonic to juvenile stages for 52 days). The results demonstrated that seawater acidification promoted otolith growth (mass and size) but did not change their geometric outlines. Seawater acidification did not alter the somatic growth or otolith elemental incorporation (Sr, Ba and Mg) in the flounder. Seawater acidification increased the occurrence of abnormally developed calcitic otoliths (calcite) which considerably differed from the aragonitic otoliths in surface and crystal structures. Additionally, elemental incorporation (Sr:Ca and Ba:Ca) appeared to be higher in aragonitic otoliths than in calcitic otoliths, which was likely related to their unique manners of formation. Our results agreed with the broad literature, in that seawater acidification showed species-specific influences (positive or no effect) on otolith size but did not affect somatic growth, otolith shape or elemental incorporation of fish at ELSs. These findings provide knowledge for evaluating the ecological effects of ocean acidification on the recruitment and population dynamics of fish in the wild.

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Reanalysis shows the extreme decline effect does not exist in fish ocean acidification studies

Contradictory Results

A meta-analysis published in PLoS Biology by Clements et al. (2022) claims there is an extreme decline effect in studies published between 2009-2019 on the impacts of ocean acidification (OA) on fish behaviour. Here I show that the extreme decline effect reported by Clements et al. is a statistical artifact caused by the way they corrected for zero values in percentage data, which was more common in the earliest experiments compared with later studies. Furthermore, selective choices for excluding or including data, along with serious errors in the compilation of data and missing studies with strong effects, weakened the effect sizes reported for papers after 2010, further exacerbating the decline effect reported by Clements et al. When the data is reanalyzed using appropriate corrections for zero values in percentage and proportional data, and using a complete, corrected and properly screened data set, the extreme decline effect reported by Clements et al. no longer exists.

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Predicted future changes in ocean temperature and pH do not affect prey selection by the girdled dogwhelk Trochia cingulata

Predator–prey relationships can drive community dynamics in marine systems, but it remains unclear how future changes in seawater temperatures and pH will influence these relationships. This study assessed the effect of predicted future temperatures and pH on the prey choice of the girdled dogwhelk Trochia cingulata (family Muricidae) when offered native (Aulacomya atraChoromytilus meridionalis) and alien (Semimytilus algosus) mussels. Whelks were exposed to three pH levels: 8.0 (current), 7.7 (intermediate) and 7.5 (extreme), at each of three temperatures: 9 °C (cooling), 13 °C (current) and 17 °C (warming) for 6 weeks. Thereafter, the prey preference and predation rate were compared among treatments. Within two weeks, 98% of whelks exposed to warming died, precluding assessment of how warming affects their prey preference. Despite high mortality, the highest predation rates were recorded at 17 °C regardless of the pH level, likely reflecting increased energy costs and ingestion rates associated with warming. In the remaining treatments whelks preferred S. algosus irrespective of the levels of seawater cooling or acidification. These results align with previous work that demonstrated a preference by T. cingulata for S. algosus and suggest that the predator–prey relationship between this whelk and its mussel prey is unlikely to be disrupted under future marine conditions.

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Effects of seawater acidification on echinoid adult stage: a review

The continuous release of CO2 in the atmosphere is increasing the acidity of seawater worldwide, and the pH is predicted to be reduced by ~0.4 units by 2100. Ocean acidification (OA) is changing the carbonate chemistry, jeopardizing the life of marine organisms, and in particular calcifying organisms. Because of their calcareous skeleton and limited ability to regulate the acid–base balance, echinoids are among the organisms most threatened by OA. In this review, 50 articles assessing the effects of seawater acidification on the echinoid adult stage have been collected and summarized, in order to identify the most important aspects to consider for future experiments. Most of the endpoints considered (i.e., related to calcification, physiology, behaviour and reproduction) were altered, highlighting how various and subtle the effects of pH reduction can be. In general terms, more than 43% of the endpoints were modified by low pH compared with the control condition. However, animals exposed in long-term experiments or resident in CO2-vent systems showed acclimation capability. Moreover, the latitudinal range of animals’ distribution might explain some of the differences found among species. Therefore, future experiments should consider local variability, long-term exposure and multigenerational approaches to better assess OA effects on echinoids.

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High CO2 inhibits substratum exploration and settlement of coral larvae

Biological and physical factors affecting coral recruitment are critical in influencing the recovery of coral communities after disturbance. While ocean acidification (OA) can reduce coral settlement and the early growth of coral recruits, the impact of OA on coral larval swimming behavior is unknown. Here, we investigated the effects of elevated CO2 on the swimming behavior and settlement of coral larvae of 2 common Acropora species. Larvae were exposed to 4 CO2 partial pressure (pCO2) conditions consistent with the current Intergovernmental Panel for Climate Change predictions for the next few centuries (pCO2: 393, 853, 1485, 3022 µatm; pH: 8.1, 7.8, 7.6, 7.3) in 2 laboratory experiments. We found that bottom exploration, expressed as the proportion of A. cytherea and A. pulchra larvae present in the bottom part of experimental cylinders, decreased by 92 and 98%, respectively, from the ambient to highest CO2 treatment. When offered the choice to settle on the crustose coralline algae Titanoderma prototypum, a well-known positive settlement cue, the percentage of larvae that settled on the crustose coralline algae fragments declined rapidly as pCO2 increased, with no larvae settling in the highest CO2 treatment. These results suggest that OA may negatively affect coral recruitment via direct effects on larval swimming behavior, with larvae avoiding benthic probing in response to high CO2.

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Low-pH seawater alters indirect interactions in rocky-shore tidepools

Ocean acidification is expected to degrade marine ecosystems, yet most studies focus on organismal-level impacts rather than ecological perturbations. Field studies are especially sparse, particularly ones examining shifts in direct and indirect consumer interactions. Here we address such connections within tidepool communities of rocky shores, focusing on a three-level food web involving the keystone sea star predator, Pisaster ochraceus, a common herbivorous snail, Tegula funebralis, and a macroalgal basal resource, Macrocystis pyrifera. We demonstrate that during nighttime low tides, experimentally manipulated declines in seawater pH suppress the anti-predator behavior of snails, bolstering their grazing, and diminishing the top-down influence of predators on basal resources. This attenuation of top-down control is absent in pools maintained experimentally at higher pH. These findings suggest that as ocean acidification proceeds, shifts of behaviorally mediated links in food webs could change how cascading effects of predators manifest within marine communities.

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Swimming performance of sharks and rays under climate change

Climate change stressors (e.g., warming and ocean acidification) are an imminent challenge to the physiological performance of marine organisms. Several studies spanning the last decade have reported widespread effects of warming and acidification on marine fishes, especially teleosts, but more work is needed to elucidate the responses in marine elasmobranchs, i.e., sharks and rays. Dispersal capacity, as a result of locomotor performance, is a crucial trait that will determine which group of elasmobranchs will be more or less vulnerable to changes in the environment. In fact, efficient and high locomotor performance may determine the capacity for elasmobranchs to relocate to a more favorable area. In this review we integrate findings from work on locomotion of marine sharks and rays to identify characteristics that outline potential vulnerabilities and strength of sharks and rays under climate change. Traits such as intraspecific variability in response to climatic stressors, wide geographic range, thermotaxis, fast swimming or low energetic costs of locomotion are likely to enhance the capacity to disperse. Future studies may focus on understanding the interacting effect of climatic stressors on morphology, biomechanics and energetics of steady and unsteady swimming, across ontogeny and species.

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Elevated temperature and low pH affect the development, reproduction, and feeding preference of the tropical cyclopoid copepod Oithona rigida

The copepod genus Oithona is among the most abundant mesozooplankton in both eutrophic and oligotrophic waters. This paper reports the individual and combined effect of temperature and pH on the development, reproduction success, and feeding preference of the tropical species Oithona rigida. Experiments were conducted at different temperature (28, 30, 31, and 32°C) and pH (7.7, 7.9, and 8.1) conditions. Effects on vital rates were observed for different developmental stages and adult males. Sex ratio varied from near 1:1 at 28°C to almost entirely female at 32°C. Egg production and hatching success were maximum at 30°C and pH at 7.9. O. rigida preferred the motile green alga Dunaliella salina in terms of ingestion rate, feed selectivity, and egg production across all the temperature and pH conditions. Long-term studies are needed to validate the adaptability of this species to a variety of climate impacts.

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GABA receptors in the olfactory epithelium of the gilthead seabream (Sparus aurata)

Exposure to high PCO2/low pH seawater induces behavioural alterations in fish; a possible explanation for this is a reversal of Cl/HCO3 currents through GABAA receptors (the GABAA receptor theory). However, the main evidence for this is that gabazine, a GABAA receptor antagonist, reverses these effects when applied to the water, assuming that exposure to systems other than the CNS would be without effect. Here, we show the expression of both metabotropic and ionotropic GABA receptors, and the presence of GABAA receptor protein, in the olfactory epithelium of gilthead seabream. Furthermore, exposure of the olfactory epithelium to muscimol (a specific GABAA receptor agonist) increases or decreases the apparent olfactory sensitivity to some odorants. Thus, although the exact function of GABAA receptors in the olfactory epithelium is not yet clear, this may complicate the interpretation of studies wherein water-borne gabazine is used to reverse the effects of high CO2 levels on olfactory-driven behaviour in fish.

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A systematic review of the behavioural changes and physiological adjustments of elasmobranchs and teleost’s to ocean acidification with a focus on sharks

In recent years, much attention has been focused on the impact of climate change, particularly via ocean acidification (OA), on marine organisms. Studying the impact of OA on long-living organisms, such as sharks, is especially challenging. When the ocean waters absorb anthropogenic carbon dioxide (CO2), slow-growing shark species with long generation times may be subjected to stress, leading to a decrease in functionality. Our goal was to examine the behavioral and physiological responses of sharks to OA and the possible impacts on their fitness and resilience. We conducted a systematic review in line with PRISMA-Analyses, of previously reported scientific experiments. We found that most studies used CO2 partial pressures (pCO2) that reflect representative concentration pathways for the year 2100 (e.g., pH ~7.8, pCO2 ~1000 μatm). Since there is a considerable knowledge gap on the effect of OA on sharks, we utilized existing data on bony fish to synthesize the available knowledge. Given the similarities between the behaviors and physiology of these two superclasses’ to changes in CO2 and pH levels, there is merit in including the available information on bony fish as well. Several studies indicated a decrease in shark fitness in relation to increased OA and CO2 levels. However, the decrease was species-specific and influenced by the intensity of the change in atmospheric CO2 concentration and other anthropogenic and environmental factors (e.g., fishing, temperature). Most studies involved only limited exposure to future environmental conditions and were conducted on benthic shark species studied in the laboratory rather than on apex predator species. While knowledge gaps exist, and more research is required, we conclude that anthropogenic factors are likely contributing to shark species’ vulnerability worldwide. However, the impact of OA on the long-term stability of shark populations is not unequivocal.

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Multiple-stressor effects of ocean acidification, warming and predation risk cues on the early ontogeny of a rocky-shore keystone gastropod


  • Snail feeding was reduced by Non-Consumptive Effects (NCEs) of a predatory crab.
  • Snail feeding was not reduced by ocean acidification (OA) and warming (OW).
  • Snail tenacity was reduced by OA but only under predatory crab NCEs.
  • Snail survival and growth were resilient to OA, OW and NCEs.


To understand how climate change stressors might affect marine organisms and support adequate projections it is important to know how multiple stressors may be modulated by the presence of other species. We evaluated the direct effects of ocean warming (OW) and ocean acidification (OA) together with non-consumptive effects (NCEs) of the predatory crab Acanthocyclus hassleri on early ontogeny fitness-related traits of the commercially important rocky-shore keystone gastropod Concholepas concholepas. We measured the response of nine traits to these stressors at either the organismal level (survival, growth, feeding rates, tenacity, metabolic rate, calcification rate) or sub-organismal level (nutritional status, ATP-supplying capacity, stress condition). C. concholepas survival was not affected by any of the stressors. Feeding rates were not affected by OW or OA; however, they were reduced in the presence of crab NCEs compared with control conditions. Horizontal tenacity was affected by the OA × NCEs interaction; in the presence of NCEs, OA reduced tenacity. The routine metabolic rate, measured by oxygen consumption, increased significantly with OW. Nutritional status assessment determined that carbohydrate content was not affected by any of the stressors. However, protein content was affected by the OA × NCEs interaction; in the absence of NCEs, OA reduced protein levels. ATP-supplying capacity, measured by citrate synthase (CS) activity, and cellular stress condition (HSP70 expression) were reduced by OA, with reduction in CS activity found particularly at the high temperature. Our results indicate C. concholepas traits are affected by OA and OW and the effects are modulated by predator risk (NCEs). We conclude that some C. concholepas traits are resilient to climate stressors (survival, growth, horizontal tenacity and nutritional status) but others are affected by OW (metabolic rate), OA (ATP-supplying capacity, stress condition), and NCEs (feeding rate). The results suggest that these negative effects can adversely affect the associated community.

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Ocean acidification, but not environmental contaminants, affects fertilization success and sperm motility in the sea urchin Paracentrotus lividus

Ocean acidification poses an increasing concern for broadcast spawning species that release gametes in the water column where fertilization occurs. Indeed, the functionality of gametes and their interactions may be negatively affected by reduced pH. Susceptibility to other environmental stressors, such as pollutants, may be also altered under acidified conditions, resulting in more detrimental effects. To verify this hypothesis, combined exposures to CO2-driven acidification and environmentally relevant concentrations (0.5 µg/L) of three contaminants (caffeine, diclofenac, and PFOS, all singularly or in mixture) were carried out to highlight potential negative effects on fertilization success and motility of sperm in the sea urchin Paracentrotus lividus. Our results showed a significant reduction in the percentage of fertilized eggs when sperm were pre-exposed to reduced pH (ambient pH minus 0.4 units) compared to that of controls (ambient, pH = 8.1). Sperm speed and motility also decreased when sperm were activated and then exposed at reduced pH. Conversely, at both pH values tested, no significant effect due to the contaminants, nor of their interaction with pH, was found on any of the biological endpoints considered.

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On the effects of temperature and pH on tropical and temperate holothurians

Ocean acidification and increased ocean heat content has direct and indirect effects on marine organisms such as holothurians (sea cucumbers) that are vulnerable to changes in pH and temperature. These environmental factors have the potential to influence organismal performance and fitness at different life stages. Tropical and temperate holothurians are more vulnerable to temperature and pH than those from colder water environments. The high level of environmental variation observed in the oceans could influence organismal responses and even produce a wide spectrum of compensatory physiological mechanisms. It is possible that in these areas, larval survival will decline by up to 50% in response to a reduction of 0.5 pH units. Such reduction in pH may trigger low intrinsic growth rates and affect the sustainability of the resource. Here we describe the individual and combined effects that temperature and pH could produce in these organisms. We also describe how these effects can scale from individuals to the population level by using age-structured spatial models in which depensation can be integrated. The approach shows how physiology can improve the conservation of the resource based on the restriction of growth model parameters and by including a density threshold, below which the fitness of the population, specifically intrinsic growth rate, decreases.

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Meta-analysis reveals an extreme “decline effect” in the impacts of ocean acidification on fish behavior

Ocean acidification—decreasing oceanic pH resulting from the uptake of excess atmospheric CO2—has the potential to affect marine life in the future. Among the possible consequences, a series of studies on coral reef fish suggested that the direct effects of acidification on fish behavior may be extreme and have broad ecological ramifications. Recent studies documenting a lack of effect of experimental ocean acidification on fish behavior, however, call this prediction into question. Indeed, the phenomenon of decreasing effect sizes over time is not uncommon and is typically referred to as the “decline effect.” Here, we explore the consistency and robustness of scientific evidence over the past decade regarding direct effects of ocean acidification on fish behavior. Using a systematic review and meta-analysis of 91 studies empirically testing effects of ocean acidification on fish behavior, we provide quantitative evidence that the research to date on this topic is characterized by a decline effect, where large effects in initial studies have all but disappeared in subsequent studies over a decade. The decline effect in this field cannot be explained by 3 likely biological explanations, including increasing proportions of studies examining (1) cold-water species; (2) nonolfactory-associated behaviors; and (3) nonlarval life stages. Furthermore, the vast majority of studies with large effect sizes in this field tend to be characterized by low sample sizes, yet are published in high-impact journals and have a disproportionate influence on the field in terms of citations. We contend that ocean acidification has a negligible direct impact on fish behavior, and we advocate for improved approaches to minimize the potential for a decline effect in future avenues of research.

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Ocean warming and acidification degrade shoaling performance and lateralization of novel tropical–temperate fish shoals

Gregarious behaviours are common in animals and provide various benefits such as food acquisition and protection against predators. Many gregarious tropical species are shifting poleward under current ocean warming, creating novel species and social interactions with local temperate taxa. However, how the dynamics of these novel shoals might be altered by future ocean warming and acidification remains untested. Here we evaluate how novel species interactions, ocean acidification and warming affect shoaling dynamics, motor lateralization and boldness of range-extending tropical and co-shoaling temperate fishes under controlled laboratory conditions. Fishes were exposed to 1 of 12 treatments (combinations of three temperature levels, two pCO2 levels and two shoal type levels: mixed species or temperate only) for 38 days. Lateralization (a measure of asymmetric expression of cognitive function in group coordination and predator escape) of tropical and temperate species was right-side biased under present-day conditions, but side bias significantly diminished in tropical and temperate fishes under ocean acidification. Ocean acidification also decreased shoal cohesion irrespective of shoaling type, with mixed-species shoals showing significantly lower cohesion than temperate-only shoals irrespective of climate stressors. Tropical fish became bolder under ocean acidification (after 4 weeks), and temperate fish became bolder with increasing temperature, while ocean acidification dampened temperate fish boldness. Our findings highlight the direct effect of climate stressors on fish behaviour and the interplay with the indirect effects of novel species interactions. Because strong shoal cohesion and lateralization are key determinants of species fitness, their degradation under ocean warming and acidification could adversely affect species performance in novel assemblages in a future ocean, and might slow down tropical species range extensions.

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Molecular basis of parental contributions to the behavioural tolerance of elevated pCO2 in a coral reef fish

Knowledge of adaptive potential is crucial to predicting the impacts of ocean acidification (OA) on marine organisms. In the spiny damselfish, Acanthochromis polyacanthus, individual variation in behavioural tolerance to elevated pCO2 has been observed and is associated with offspring gene expression patterns in the brain. However, the maternal and paternal contributions of this variation are unknown. To investigate parental influence of behavioural pCO2 tolerance, we crossed pCO2-tolerant fathers with pCO2-sensitive mothers and vice versa, reared their offspring at control and elevated pCO2 levels, and compared the juveniles’ brain transcriptional programme. We identified a large influence of parental phenotype on expression patterns of offspring, irrespective of environmental conditions. Circadian rhythm genes, associated with a tolerant parental phenotype, were uniquely expressed in tolerant mother offspring, while tolerant fathers had a greater role in expression of genes associated with histone binding. Expression changes in genes associated with neural plasticity were identified in both offspring types: the maternal line had a greater effect on genes related to neuron growth while paternal influence impacted the expression of synaptic development genes. Our results confirm cellular mechanisms involved in responses to varying lengths of OA exposure, while highlighting the parental phenotype’s influence on offspring molecular phenotype.

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Integrative assessment of sediments affected by CO2 enrichment: a case study in the Bay of Santos—SP, Brazil

CO2 enrichment in the marine environment caused by leakages from carbon capture and storage technologies may occur over operational procedures. An integrated approach using weight-of-evidence was applied to assess the environmental risk associated with the acidification caused by CO2 enrichment in coastal sediments from Santos (Brazil). Chemical analyses (metal(loid)s and organic contaminant (e.g., hydrocarbons), toxicity tests (amphipods mortality, sea-urchin embryo-larval development) and macro-benthic community structure alteration assessment were performed with different acidified scenarios (pH 8.0–6.0) for two stations with different contamination degrees. These lines of evidence were statistically analyzed and integrated (multivariate analysis and ANOVA). Results of toxicity showed significant chronic effects starting at pH 7.0 while acute effects were observed starting at pH 6.5. The macro-benthic community integrity showed significant differences for all treatments at the Piaçaguera channel station, considered to be moderately contaminated. Results from the multivariate analysis correlated toxic effects and increase in the mobility of some elements with acidification. Also, the biological indexes were correlated with concentrations of dissolved Zn in seawater. The pH of 6.0 was extremely toxic for marine life due to its high acidification and metal bioavailability. The approach herein identified and discriminated the origin of the degradation caused by the acidification related to the enrichment of CO2.

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Behavioural stress propagation in benthic invertebrates caused by acute pH drop-induced metabolites

Studies on pH stress in marine animals typically focus on direct or species-specific aspects. We here test the hypothesis that a drop to pH = 7.6 indirectly affects the intra- and interspecific interactions of benthic invertebrates by means of chemical communication. We recorded fitness-relevant behaviours of small hermit crabs Diogenes pugilator, green shore crabs Carcinus maenas, and harbour ragworms Hediste diversicolor in response to short-term pH drop, and to putative stress metabolites released by conspecifics or gilt-head sea bream Sparus aurata during 30 min of acute pH drop. Not only did acute pH drop itself impair time to find a food cue in small hermit crabs and burrowing in harbour ragworms, but similar effects were observed under exposure to pH drop-induced stress metabolites. Stress metabolites from S. aurata, but not its regular control metabolites, also induced avoidance responses in all recipient species. Here, we confirm that a short-term abrupt pH drop, an abiotic stressor, has the capacity to trigger the release of metabolites which induce behavioural responses in conspecific and heterospecific individuals, which can be interpreted as a behavioural cost. Our findings that stress responses can be indirectly propagated through means of chemical communication warrant further research to confirm the effect size of the behavioural impairments caused by stress metabolites and to characterise their chemical nature.

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Who wins or loses matters: strongly interacting consumers drive seagrass resistance under ocean acidification


  • Ocean acidification (OA) directly facilitated algal epiphyte and seagrass.
  • Co-occurring grazers variably controlled algal overgrowth on seagrass.
  • pH-tolerant, strongly interacting grazers maintained overall grazing pressure.
  • Grazing and OA additively increased seagrass productivity.


Global stressors are increasingly altering ecosystem resistance, resilience, and functioning by reorganizing vital species interactions. However, our predictive understanding of these changes is hindered by failures to consider species-specific functional roles and stress responses within communities. Stressor-driven loss or reduced performance of strongly interacting species may generate abrupt shifts in ecosystem states and functions. Yet, empirical support for this prediction is scarce, especially in marine climate change research. Using a marine assemblage comprising a habitat-forming seagrass (Phyllospadix torreyi), its algal competitor, and three consumer species (algal grazers) with potentially different functional roles and pH tolerance, we investigated how ocean acidification (OA) may, directly and indirectly, alter community resistance. In the field and laboratory, hermit crabs (Pagurus granosimanus and P. hirsutiusculus) and snails (Tegula funebralis) displayed distinct microhabitat use, with hermit crabs more frequently grazing in the area of high algal colonization (i.e., surfgrass canopy). In mesocosms, this behavioral difference led to hermit crabs exerting ~2 times greater per capita impact on algal epiphyte biomass than snails. Exposure to OA variably affected the grazers: snails showed reduced feeding and growth under extreme pH (7.3 and 7.5), whereas hermit crabs (P. granosimanus) maintained a similar grazing rate under all pH levels (pH 7.3, 7.5, 7.7, and 7.95). Epiphyte biomass increased more rapidly under extreme OA (pH 7.3 and 7.5), but natural densities of snails and hermit crabs prevented algal overgrowth irrespective of pH treatments. Finally, grazers and acidification additively increased surfgrass productivity and delayed the shoot senescence. Hence, although OA impaired the function of the most abundant consumers (snails), strongly interacting and pH-tolerant species (hermit crabs) largely maintained the top-down pressure to facilitate seagrass dominance. Our study highlights significant within-community variation in species functional and response traits and shows that this variation has important ecosystem consequences under anthropogenic stressors.

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Molecular mechanisms of sperm motility are conserved in an early-branching metazoan


Reef-building corals are the keystone species of the world’s most biodiverse yet threatened marine ecosystems. Coral reproduction, critical for reef resilience, requires that coral sperm swim through the water column to reach the egg. However, little is known about the mechanisms that regulate coral sperm motility. We found here that coral sperm motility is pH dependent and that activation of motility requires signaling via the pH-sensing enzyme soluble adenylyl cyclase. This study reveals the deep conservation of a sperm activation pathway from humans to corals, presenting the first comprehensive examination of the molecular mechanisms regulating sperm motility in an early-diverging animal. These results are critical for understanding the resilience of this sensitive life stage to a changing marine environment.


Efficient and targeted sperm motility is essential for animal reproductive success. Sperm from mammals and echinoderms utilize a highly conserved signaling mechanism in which sperm motility is stimulated by pH-dependent activation of the cAMP-producing enzyme soluble adenylyl cyclase (sAC). However, the presence of this pathway in early-branching metazoans has remained unexplored. Here, we found that elevating cytoplasmic pH induced a rapid burst of cAMP signaling and triggered the onset of motility in sperm from the reef-building coral Montipora capitata in a sAC-dependent manner. Expression of sAC in the mitochondrial-rich midpiece and flagellum of coral sperm support a dual role for this molecular pH sensor in regulating mitochondrial respiration and flagellar beating and thus motility. In addition, we found that additional members of the homologous signaling pathway described in echinoderms, both upstream and downstream of sAC, are expressed in coral sperm. These include the Na+/H+ exchanger SLC9C1, protein kinase A, and the CatSper Ca2+ channel conserved even in mammalian sperm. Indeed, the onset of motility corresponded with increased protein kinase A activity. Our discovery of this pathway in an early-branching metazoan species highlights the ancient origin of the pH-sAC-cAMP signaling node in sperm physiology and suggests that it may be present in many other marine invertebrate taxa for which sperm motility mechanisms remain unexplored. These results emphasize the need to better understand the role of pH-dependent signaling in the reproductive success of marine animals, particularly as climate change stressors continue to alter the physiology of corals and other marine invertebrates.

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