Posts Tagged 'reproduction'

Sperm motility impairment in free spawning invertebrates under near-future level of ocean acidification: uncovering the mechanism

Ocean acidification (OA) refers to the decrease in ocean water pH resulting from the increasing absorption of atmospheric CO2. This will cause changes in the ocean’s carbonate chemistry system with a resulting impact on reproduction of marine organisms. Reproduction is the fundamental process that allows the conservation of the species; in free-spawning marine invertebrates, this process is highly sensitive to changes in seawater quality and chemistry. To date, the majority of the studies concerned OA effects on reproduction has been focused on embryo and larval development. Despite several evidence for the impairment of reproductive success by environmental perturbations through altering gamete quality, sperm physiological responses to OA are poorly investigated. In this study, we evaluated the effects of exposure to acidified seawater (AcSW) (pH 7.8), which approximate the predicted global averages for oceanic surface waters at the end of this century, on sperm quality of the mussel Mytilus galloprovincialis and the ascidian Ciona robusta by evaluating several endpoints, such as motility, vitality, mitochondrial activity, oxidative state, and intracellular pH (pHi). Following sperm exposure to AcSW, the percentage of motile spermatozoa, mitochondrial activity and pHi decreased in comparison to the current seawater pH of 8.1, whereas vitality and oxidative state were unaffected by the low external pH in both the species. In broadcast spawners, a relationship between sperm intracellular pH and the initiation of motility are well known. Spermatozoa are immotile in the testes and motility is induced after the spermatozoa are released into seawater; the alkaline pH of seawater, in fact, increases the pHi activating motility and mitochondrial respiration. The results of this study suggest that the lowering of seawater pH as predicted to occur for 2100, through the inhibition of pHi increase, prevent sperm motility activation. Sperm motility is a key determinant of fertilization success; consequently, a corresponding drop in fertilization success would be expected with important implications for the fitness and the survival of marine invertebrates.

Continue reading ‘Sperm motility impairment in free spawning invertebrates under near-future level of ocean acidification: uncovering the mechanism’

Intra-specific variation of ocean acidification effects in marine mussels and oysters: integrative physiological studies on tissue and organism responses

Uptake of increasing anthropogenic CO2 emissions by ocean surface waters is causing an increase of seawater PCO2 accompanied by a decrease of seawater pH and carbonate ion concentrations. This process, termed ocean acidification (OA), is predicted to negatively affect many marine organisms with likely consequences for marine ecosystems and the services they provide. Calcifying mussels and oysters, and particularly their early life stages, are predicted to be among the most OA sensitive taxa, as OA interferes with the calcification process. In addition, mussels and oysters possess a relatively low ability to compensate for CO2 induced disturbances in extracellular body fluid pH with potential physiological downstream effects such as elevated metabolic maintenance costs. As mussels and oysters are key habitat forming organisms in many highly productive temperate coastal communities, negative OA effects may translate into deleterious effects at an ecosystem scale. In particular, the relative long generation time of most marine bivalves raises the concern that the rapid rate at which OA occurs may outpace species’ ability to genetically adapt, leaving pre-existing genetic variation as a potential key to species resilience under OA. Against this backdrop, this thesis contributes to the understanding of physiological mechanisms that underpin and define the OA vulnerability of ecologically and economically important mussels and oysters. Thereby, emphasis was placed on investigating intra-specific variance as a proxy for potential adaptive capacities. Kiel Fjord is located in the Western Baltic Sea and is characterised by strong seasonal and diurnal fluctuations in seawater PCO2. These fluctuations are caused by upwelling events of acidified bottom waters with peak PCO2 values (>2300 μatm) that are already by far exceeding those projected for open ocean surface waters by the end of this century. Despite these unfavourable conditions, blue mussels (Mytilus edulis) dominate the benthic community, which makes this population particularly interesting in the context of metabolic adaptation to OA. Consequently, a long-term multi-generation CO2 acclimation experiment with different family lines of M. edulis from Kiel Fjord formed the first part of this thesis. Offspring of 16 different family lines were transferred to three different PCO2 conditions, representing present and predicted PCO2 levels in Kiel Fjord (700 μatm (control), 1120 μatm (intermediate) and 2400 μatm (high)). Larval survival rates were substantially different between family lines at the highest PCO2 level. Based on these differences, families were classified as either ‘tolerant’ (i.e. successful settlement at all PCO2 levels) or ‘sensitive’ (i.e. successful settlement only at control and intermediate PCO2 level). Subsequently, the offspring were raised for over one year at respective PCO2 levels, followed by measurements of physiological parameters at the whole-animal, tissue (gill and outer mantle) and biochemical level (key metabolic enzymes). The results revealed that routine metabolic rates (RMR) and summed tissue respiration were increased in tolerant families at intermediate PCO2, indicating elevated homeostatic costs. However, this higher energy demand at the intermediate PCO2 level was not accompanied by a simultaneous increase in energy assimilation (i.e. clearance rates (CR)), indicating an incipient imbalance in energy demand and supply. Consequently, RMRs at the highest PCO2 were not different to control RMRs but associated with reduced CRs, which correlated with a lower gill metabolic scope, reduced gill mitochondrial capacities (lower capacities for citrate synthase (CS) and cytochrome c oxidase (COX)) as well as an increased capacity for anaerobic energy production (lower ratio of pyruvate kinase to phospoenolpyruvate carboxykinase). In conjunction with a lower COX to CS ratio observed in outer mantle tissue, this suggested a CO2-induced shift of metabolic pathways in tolerant families at the highest PCO2 level. By contrast, sensitive families had an unchanged RMR, tissue respiration and CR at the intermediate CO2. However, a higher control RMR in sensitive than tolerant families at similar CR suggested a lower, CO2 independent metabolic efficiency in sensitive families. This was also reflected in their lower gill mitochondrial scope at control conditions compared to tolerant families. These findings suggested that sensitive families lack the metabolic scope to cover OA induced higher maintenance costs and have to rely on energy reallocation and thus, energy trade-offs which may also have prevented survival at the highest experimental PCO2 level. Accordingly, investigations of 3-hydroxyacyl-CoA dehydrogenase (HADH) capacities, which catalyses a key step in lipid oxidation, suggested an increased reliance on lipids as metabolic fuel in sensitive families at elevated PCO2. If this was also prevalent during the larval phase, a quicker depletion of lipid reserves before completion of metamorphosis may have contributed to the higher larval mortality at the highest PCO2 treatment in sensitive compared to tolerant mussels. The second part of the thesis aimed to clarify whether a higher OA tolerance in Sydney rock oysters (Saccostrea glomerata) is directly correlated with an increased capacity to compensate for CO2 induced extracellular acid-base disturbances, and whether such a capacity is driven by higher metabolic and ion-regulatory costs at the tissue level. Earlier studies focusing on two different populations of Sydney rock oysters demonstrated that oysters that were selectively bred for increased growth and disease resistance (‘selected oysters’) have a higher CO2 resilience compared to the wild population (‘wild oysters’). To unravel the underlying physiological mechanisms, oysters of both populations were acclimated at control and elevated PCO2 (1100 μatm) levels for seven weeks, followed by determinations of extracellular acidbase parameters (pHe, PeCO2, [HCO3 -]e), tissue respiration and indirect determination of energy demands of major ion regulatory transport proteins. Indeed, at elevated PCO2, wild oysters had a lower pHe and an increased PeCO2 whereas extracellular acid-base status of selected oysters remained unaffected. However, differing pHe values between oyster types were not driven by elevated metabolic costs of major ion regulators at tissue level. Selected oysters rather exhibited an increased systemic capacity to eliminate metabolic CO2, which likely came through higher and energetically more efficient filtration rates and associated facilitation of gas exchange, suggesting that effective filtration and CO2 resilience might be positively correlated traits in oysters. In conclusion, the findings of this thesis contribute to the growing evidence that ongoing OA will likely impair the physiology of marine mussels and oysters with potentially associated downstream consequences for the respective ecosystems. However, the results also suggest adaptive capacities in both species studied. The higher CO2 resilience of selected Sydney rock oysters was expressed within the – in evolutionary terms – rapid time span of only a few generations of selective breeding, which indicates that rapid adaptation to OA may be possible in marine bivalves. The observed intra-specific variation of OA responses in blue mussels suggests standing genetic variation within this population, which is likely to be key for the persistence of populations under rapidly occurring OA. However, as global change is not limited to OA, future research will have to reassess potential resilience traits and adaptive capacities to OA when combined with changes in other environmental drivers.

Continue reading ‘Intra-specific variation of ocean acidification effects in marine mussels and oysters: integrative physiological studies on tissue and organism responses’

A coralline alga gains tolerance to ocean acidification over multiple generations of exposure

Crustose coralline algae play a crucial role in the building of reefs in the photic zones of nearshore ecosystems globally, and are highly susceptible to ocean acidification. Nevertheless, the extent to which ecologically important crustose coralline algae can gain tolerance to ocean acidification over multiple generations of exposure is unknown. We show that, while calcification of juvenile crustose coralline algae is initially highly sensitive to ocean acidification, after six generations of exposure the effects of ocean acidification disappear. A reciprocal transplant experiment conducted on the seventh generation, where half of all replicates were interchanged across treatments, confirmed that they had acquired tolerance to low pH and not simply to laboratory conditions. Neither exposure to greater pH variability, nor chemical conditions within the micro-scale calcifying fluid internally, appeared to play a role in fostering this capacity. Our results demonstrate that reef-accreting taxa can gain tolerance to ocean acidification over multiple generations of exposure, suggesting that some of these cosmopolitan species could maintain their critical ecological role in reef formation.

Continue reading ‘A coralline alga gains tolerance to ocean acidification over multiple generations of exposure’

Antagonistic interplay between pH and food resources affects copepod traits and performance in a year-round upwelling system

Linking pH/pCO2 natural variation to phenotypic traits and performance of foundational species provides essential information for assessing and predicting the impact of ocean acidification (OA) on marine ecosystems. Yet, evidence of such linkage for copepods, the most abundant metazoans in the oceans, remains scarce, particularly for naturally corrosive Eastern Boundary Upwelling systems (EBUs). This study assessed the relationship between pH levels and traits (body and egg size) and performance (ingestion rate (IR) and egg reproduction rate (EPR)) of the numerically dominant neritic copepod Acartia tonsa, in a year-round upwelling system of the northern (23° S) Humboldt EBUs. The study revealed decreases in chlorophyll (Chl) ingestion rate, egg production rate and egg size with decreasing pH as well as egg production efficiency, but the opposite for copepod body size. Further, ingestion rate increased hyperbolically with Chl, and saturated at ~1 µg Chl. L−1. Food resources categorized as high (H, >1 µg L−1) and low (L,  7.89) and future (>400 µatm pCO2, pH < 7.89) were used to compare our observations to values globally employed to experimentally test copepod sensitivity to OA. A comparison (PERMANOVA) test with Chl/pH (2*2) design showed that partially overlapping OA levels expected for the year 2100 in other ocean regions, low-pH conditions in this system negatively impacted traits and performance associated with copepod fitness. However, interacting antagonistically with pH, food resource (Chl) maintained copepod production in spite of low pH levels. Thus, the deleterious effects of ocean acidification are modulated by resource availability in this system.

Continue reading ‘Antagonistic interplay between pH and food resources affects copepod traits and performance in a year-round upwelling system’

Experimental acidification increases susceptibility of Mercenaria mercenaria to infection by Vibrio species

Highlights

• Clams in high pCO2/low pH were more susceptible to infection by pathogenic Vibrios.

• Growth and abundance of Vibrio spp. were greater under high pCO2/low pH.

• Clams reared under high pCO2/low pH seemed to have a broad tolerance range for pH.

• Long-term effect of acidification and susceptibility to vibriosis is understudied.

Abstract

Ocean acidification alters seawater carbonate chemistry, which can have detrimental impacts for calcifying organisms such as bivalves. This study investigated the physiological cost of resilience to acidification in Mercenaria mercenaria, with a focus on overall immune performance following exposure to Vibrio spp. Larval and juvenile clams reared in seawater with high pCO2 (∼1200 ppm) displayed an enhanced susceptibility to bacterial pathogens. Higher susceptibility to infection in clams grown under acidified conditions was derived from a lower immunity to infection more so than an increase in growth of bacteria under high pCO2. A reciprocal transplant of juvenile clams demonstrated the highest mortality amongst animals transplanted from low pCO2/high pH to high pCO2/low pH conditions and then exposed to bacterial pathogens. Collectively, these results suggest that increased pCO2 will result in immunocompromised larvae and juveniles, which could have complex and pernicious effects on hard clam populations.

Continue reading ‘Experimental acidification increases susceptibility of Mercenaria mercenaria to infection by Vibrio species’

Negative effects of diurnal changes in acidification and hypoxia on early-life stage estuarine fishes

Estuaries serve as important nursery habitats for various species of early-life stage fish, but can experience cooccurring acidification and hypoxia that can vary diurnally in intensity. This study examines the effects of acidification (pH 7.2–7.4) and hypoxia (dissolved oxygen (DO) ~ 2–4 mg L−1) as individual and combined stressors on four fitness metrics for three species of forage fish endemic to the U.S. East Coast: Menidia menidia, Menidia beryllina, and Cyprinodon variegatus. Additionally, the impacts of various durations of exposure to these two stressors was also assessed to explore the sensitivity threshold for larval fishes under environmentally-representative conditions. C. variegatus was resistant to chronic low pH, while M. menidia and M. beryllina experienced significantly reduced survival and hatch time, respectively. Exposure to hypoxia resulted in reduced hatch success of both Menidia species, as well as diminished survival of M. beryllina larvae. Diurnal exposure to low pH and low DO for 4 or 8 h did not alter survival of M. beryllina, although 8 or 12 h of daily exposure through the 10 days posthatch significantly depressed larval size. In contrast, M. menidia experienced significant declines in survival for all intervals of diel cycling hypoxia and acidification (4–12 h). Exposure to 12-h diurnal hypoxia generally elicited negative effects equal to, or of greater severity, than chronic exposure to low DO at the same levels despite significantly higher mean DO exposure concentrations. This evidences a substantial biological cost to adapting to changing DO levels, and implicates diurnal cycling of DO as a significant threat to fish larvae in estuaries. Larval responses to hypoxia, and to a lesser extent acidification, in this study on both continuous and diurnal timescales indicate that estuarine conditions throughout the spawning and postspawn periods could adversely affect stocks of these fish, with diverse implications for the remainder of the food web.

Continue reading ‘Negative effects of diurnal changes in acidification and hypoxia on early-life stage estuarine fishes’

The effects of aragonite saturation state on hatchery-reared larvae of the greenshell mussel Perna canaliculus

The major cultured mussel species Perna canaliculus is now supported by hatchery production, providing the opportunity to explore and optimize environmental parameters to enhance production. Other cultured bivalve larvae have demonstrated performance that is directly correlated to the aragonite saturation state (Ωar) of their tank water, with low or undersaturated water being detrimental and artificially elevated Ωar enhancing productivity. Trials were, therefore, designed to specifically explore Ωar sensitivity in preveliger (0–2 days old, prodissoconch I = “PD1″) and veliger (2–21 days old, prodissoconch II = “PD2″) stages of P. canaliculus separately. For the PD1 experiment, commercial incubation tanks (control Ωar 1.9) were modified to target Ωar 0.5 or 0.8 by elevating pCO2, or 2.9, 4.5, and ∼7 by the addition of sodium carbonate. In the control environment, 72.8% ± 2.9% of fertilized eggs formed viable “D” veligers within two days; an increased yield of 82.6% ± 3.8% in Ωar 4.5 was found to be nonsignificant. In comparison, only 12.7% of the Ωar ∼7 and <1% of the Ωar 0.5 and 0.8 eggs attained the veliger stage, with the remaining underdeveloped or malformed. By 2 days postfertilization, reactive oxygen species were significantly elevated in the undersaturated treatments, whereas DNA damage, lipid hydroperoxides, and protein carbonyls were significantly higher in the Ωar 0.5 and ∼7 treatments. Antioxidant enzyme levels were significantly lower in these extreme treatments, whereas Ωar 4.5 larvae showed elevated superoxide dismutase, glutathione reductase, and peroxidase levels. Carry-over effects persisted when veligers were transferred to control conditions, with no net recruitment from undersaturated Ωar, 29.4% of eggs surviving to pediveliger under control conditions, compared with 33.2% following Ωar 4.5 exposure or 1.9% from Ωar ∼7. In the PD2 veliger trial, linear shell growth halved in undersaturated water, but was unaffected by elevation of Ωar. Mortality rate was consistent across all treatments, suggesting relative resilience to different Ωar. It is recommended that hatcheries trial Ωar 4–4.5 enrichment in preveliger incubation water to improve yield and minimize oxidative stress. Preveliger stages present a potential survival bottleneck, and focused research exploring sensitivity to near-future ocean acidification is, therefore, needed.

Continue reading ‘The effects of aragonite saturation state on hatchery-reared larvae of the greenshell mussel Perna canaliculus’


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