Emergent effects of global change on consumption depend on consumers and their resources in marine systems

A better understanding of how environmental change will affect species interactions would significantly aid efforts to scale up predictions of near-future responses to global change from individuals to ecosystems. To address this need, we used meta-analysis to quantify the individual and combined effects of ocean acidification (OA) and warming on consumption rates of predators and herbivores in marine ecosystems. Although the primary studies demonstrated that these environmental variables can have direct effects on consumers, our analyses highlight high variability in consumption rates in response to OA and warming. This variability likely reflects differences in local adaptation among species, as well as important methodological differences. For example, our results suggest that exposure of consumers to OA reduces consumption rates on average, yet consumption rates actually increase when both consumers and their resource(s) are concurrently exposed to the same conditions. We hypothesize that this disparity is due to increased vulnerability of prey or resource(s) in conditions of OA that offset declines in consumption. This hypothesis is supported by an analysis demonstrating clear declines in prey survival in studies that exposed only prey to future OA conditions. Our results illustrate how simultaneous OA and warming produce complex outcomes when species interact. Researchers should further explore other potential sources of variation in response, as well as the prey-driven component of any changes in consumption and the potential for interactive effects of OA and warming.

Numerous studies have demonstrated direct effects of ocean acidification (OA) and warming on organismal physiology and performance (1, 2), yet forecasting the emergent ecological effects of environmental change on communities remains a challenge due to the complexity of interactions between species (3–5) and stressors (1, 2, 6–8) in functioning ecosystems. Species interactions have the potential to drive shifts in communities (5, 9–11) or buffer them (5, 12, 13) from environmental change. For example, environmentally mediated increases in growth of some algal species can lead to ecosystem shifts if they outcompete or overgrow other species (14). However, environmentally mediated increases in consumption rates of key herbivores have the potential to limit this overgrowth of algae and the associated community shift (13). Indeed, authors of several of the studies that have revealed potential emergent effects of OA (14–16) or warming (17, 18) on entire marine communities attributed the observed responses at least in part to changes in species interactions. In addition, pronounced shifts in species assemblages and ecosystems during natural, large-scale warming events are often linked to modified species interactions (19, 20). Establishing general patterns of environmental control on species interactions has thus been proposed as a promising avenue for scaling up the effects of environmental change from individuals to ecosystems (9, 21–24).Environmentally mediated changes in trophic interactions may be especially important in determining the effects of global change on ecosystems, due to their potential to have cascading effects on community structure (25, 26). OA (27, 28) and warming (29–31) are generally predicted to alter consumers’ energetic demands, although the effects on consumption will depend on the shape of the performance curves, how close current environmental temperatures are to their performance optima, the magnitude of the environmental change, and their energy allocation strategies (25). The effects of OA on consumption are more likely to vary among taxa with different traits than the effects of warming, which universally affects metabolism. For example, the effects of OA can vary with the degree of calcification or the level of mobility of a given species (1, 2). However, the ability of consumers in nature to sufficiently compensate for changes in energetic demands associated with either OA or warming through altered consumption will also depend on their prey or resources (32–34). For example, an increase in a consumer’s energetic demand could be met through increased ingestion of a given resource. Shifts in the escape response, production of physical or chemical deterrents, or the size or biomass of the resource species driven by environmental change, however, can mediate the outcome (4). Thus, deciphering the environmental controls on trophic interactions requires analysis of both the consumer- and resource-driven components of predation and herbivory in future conditions.In most studies that assess the effects of OA, warming, or both on the consumption rates of marine species, researchers use controlled laboratory experiments that are amenable to meta-analysis. In these experiments, a consumer or resource is most often exposed to current and future environmental conditions for a period of days to months. Thus, the effects measured are primarily plastic and represent an organism’s ability to acclimate physiologically or behaviorally. Often, the consumer is held in treatment conditions and given prey or a resource that has not been acclimated to the experimental conditions (defined here as consumer-only experiments). In contrast, more complex studies (e.g., multispecies mesocosms or studies focused on species interactions or community-level responses) tend to include both the consumer and its resource(s) in the experimental conditions. While the responses in these experiments still represent the physiological or behavioral acclimation of the species involved, these multispecies experiments capture potential emergent effects of environmental change on species interactions that result from the direct effects on both the consumer and the resource. Prior meta-analyses have shown that there can be important variation in the temperature sensitivity of different ecological rates, such as attack rates and escape rates that can influence the emergent effects based on variation in sensitivity among trophic roles (30). Similarly, OA has been shown to affect both predator and prey detection and behavior (35–37), as well as algal traits that could affect herbivory, such as nutritional status or chemical deterrents (37). Most rare are those studies that expose only prey or resources to experimental conditions and then test their vulnerability to predation using a predator or herbivore that is not acclimated to the experimental conditions being tested. In contrast to the consumer-only experiments, these “resource-only” experiments capture how environmental change may affect the vulnerability or palatability of species that serve as resources.Experiments also vary in the complexity of environmental manipulation. Although OA and warming are happening in concert in nature, many early studies focused on the biological effects of OA or warming in isolation. As global change biology has progressed, the focus has shifted toward multifactor studies that incorporate both OA and warming in combination (e.g., factorial experiments). These studies are critically important for forecasting emergent effects, as the combined effects of OA and warming may not be additive (1, 2). This may be especially important if OA and warming have different modes of action on marine organisms (38). Synergisms, in which the effects of OA and warming exacerbate one another, have gained the most attention because of their potential to cause dramatic ecological shifts. However, even with different modes of action, one environmental-change factor may primarily drive an organism’s overall response, leading to unexpected outcomes.We conducted a systematic review (SI Appendix, Fig. S1 and Dataset S1) to assemble a database of published studies (Dataset S2) and conduct a meta-analysis quantifying the individual and combined effects of OA and warming on consumption rates, testing for variation between predator–prey and herbivore–resource interactions. We also tested for variance in the individual and combined effects of each environmental variable on different trophic roles (i.e., studies that exposed only consumers or only resources to treatment conditions prior to measuring consumption) to provide insight on their relative importance in the overall response of predation and herbivory rates in future conditions. We then tested whether taxonomic groups or life stages of interacting organisms explain any remaining variance among underlying studies to aid interpretation and identify gaps in our knowledge that need to be addressed to move the field forward. We also quantified the effects of OA and warming on prey survival in resource-only experiments, as well as the effects on consumer preference of prey or resources raised in ambient or future conditions. Finally, to quantitatively address the potential for nonadditive effects of the combined exposure to OA and warming, we calculated the individual and interactive effects of OA and warming on consumption rates for the subset of studies that factorially manipulated both variables.     

Reduced H+ channel activity disrupts pH homeostasis and calcification in coccolithophores at low ocean pH

Coccolithophores are major producers of ocean biogenic calcite, but this process is predicted to be negatively affected by future ocean acidification scenarios. Since coccolithophores calcify intracellularly, the mechanisms through which changes in seawater carbonate chemistry affect calcification remain unclear. Here we show that voltage-gated H⁺ channels in the plasma membrane of Coccolithus braarudii serve to regulate pH and maintain calcification under normal conditions but have greatly reduced activity in cells acclimated to low pH. This disrupts intracellular pH homeostasis and impairs the ability of C. braarudii to remove H⁺ generated by the calcification process, leading to specific coccolith malformations. These coccolith malformations can be reproduced by pharmacological inhibition of H⁺ channels. Heavily calcified coccolithophore species such as C. braarudii, which make the major contribution to carbonate export to the deep ocean, have a large intracellular H⁺ load and are likely to be most vulnerable to future decreases in ocean pH.

Anthropogenic CO₂ emissions and the subsequent dissolution of CO₂ in seawater have resulted in substantial changes in ocean carbonate chemistry (1). The resultant decrease in seawater pH, termed ocean acidification, is predicted to be particularly detrimental for calcifying organisms (2). Mean global surface ocean pH is currently around 8.2 but is predicted to fall as low as 7.7 by 2100 (3) and is likely to continue to fall further in the following centuries. Present-day marine organisms can experience significant fluctuations in seawater pH, particularly in coastal and upwelling regions (4, 5). Ocean acidification is therefore predicted to have an important influence not only on mean surface ocean pH but also on the extremes of pH experienced by marine organisms (6, 7).Coccolithophores (Haptophyta) are a group of globally distributed unicellular phytoplankton that are characterized by their covering of intricately formed calcite scales (coccoliths). Coccolithophores account for a significant proportion of ocean productivity and are the main producers of biogenic calcite, making major contributions to global biogeochemical cycles, including the long-term export of both inorganic and organic carbon from the ocean photic zone to deep waters (8, 9). Unlike the vast majority of calcifying organisms, coccolithophore calcification occurs in an intracellular compartment, the Golgi-derived coccolith vesicle (CV), effectively isolating the calcification process from direct changes in seawater carbonate chemistry. Nevertheless, extensive laboratory observations indicate that ocean acidification may negatively impact coccolithophore calcification, albeit with significant variability of responses between species and strains (10–14). The negative impact on calcification rates occurs at calcite saturation states (Ω_calcite) >1, indicating that it results primarily from impaired cellular production rather than dissolution (10, 15). However, prediction of how natural coccolithophore populations may respond to future changes in ocean pH are hampered by lack of mechanistic understanding of pH impacts at the cellular level (10).As calcification occurs intracellularly using external HCO₃⁻ as the primary dissolved inorganic carbon (DIC) source (16–18), coccolith formation is not directly dependent on external CO₃²⁻ concentrations. However, the uptake of HCO₃⁻ as a substrate for calcification results in the equimolar production of CaCO₃ and H⁺ in the CV (18). In order to maintain saturation conditions for calcite formation, H⁺ produced by the calcification process must be rapidly removed from the CV, placing extraordinary demands for cellular pH regulation to prevent cellular acidosis (18).Lower calcification rates under ocean acidification conditions appear to be primarily due to decreased pH rather than other aspects of carbonate chemistry (10, 19, 20). Coccolithophores exhibit highly unusual membrane physiology, including the presence of voltage-gated H⁺ channels in the plasma membrane (21) and a high sensitivity of cytosolic pH (pH_cyt) to changes in external pH (pH_o) (21, 22). Voltage-gated H⁺ channels are associated with rapid H⁺ efflux in a number of specialized animal cell types (23) and contribute to effective pH regulation in coccolithophores (21). As H⁺ channel function is dependent on the electrochemical gradient of H⁺ across the plasma membrane, this mechanism could be impaired under lower seawater pH. However, it remains unknown whether H⁺ channels play a direct role in removal of calcification-derived H⁺ or contribute to the sensitivity of coccolithophores to ocean acidification.Coccolithophores exhibit significant diversity in their extent of calcification (SI Appendix, Fig. S1). The ratio of particulate inorganic carbon to particulate organic carbon (PIC/POC) of a coccolithophore culture is a measure of the relative rates of inorganic carbon fixation by calcification and organic carbon fixation by photosynthesis, respectively, and is commonly used as a simple metric to define the degree of calcification. The abundant bloom-forming species Emiliania huxleyi is moderately calcified (PIC/POC of around 1) and has been the focus of the vast majority of the studies into the effects of environmental change in coccolithophores (13). Coastal species belonging to the Pleurochrysidaceae and Hymenomonadaceae are lightly calcified, commonly exhibiting a PIC/POC of less than 0.5 (24–27). Species such as Coccolithus braarudii, Calcidiscus leptoporus, and Helicosphaera carteri exhibit much higher PIC/POC ratios and contribute the majority of carbonate export to the deep ocean in many areas (28–30). The physiological response of heavily calcified coccolithophores to ocean acidification is therefore of considerable biogeochemical significance. Growth and calcification rates in C. leptoporus and C. braarudii are sensitive to pH values predicted to prevail on a future decadal timescale (10, 15, 31, 32). However, a mechanistic understanding of the different sensitivity of coccolithophore species to changing ocean carbonate chemistry is lacking.The net H⁺ load in a cell is determined by the combination of metabolic processes that consume or produce H⁺. H⁺ fluxes in coccolithophores will be primarily determined by the balance of H⁺ consumed by photosynthesis and H⁺ generated by calcification, with uptake of different carbon sources a particularly important consideration (Fig. 1A). CO₂ uptake for photosynthesis results in no net production or consumption of H⁺, whereas uptake of HCO₃⁻ requires the equimolar consumption of H⁺ in order to generate CO₂. Growth at elevated CO₂ causes a switch from HCO₃⁻ uptake to predominately CO₂ uptake in E. huxleyi (33, 34). The associated net decrease in H⁺ consumption will therefore increase the H⁺ load in coccolithophores grown at elevated CO₂, which may exacerbate the potential for cytosolic acidosis caused by lower seawater pH.Open in a separate windowFig. 1.Physiology and H⁺ fluxes of C. braarudii cells grown at different seawater pH. (A) Schematic indicating H⁺ fluxes associated with photosynthesis and calcification in a coccolithophore cell. While many metabolic processes may contribute to the cellular H⁺ budget, these two processes are likely to be the major contributors. In a cell taking up HCO₃⁻, the overall H⁺ budget is determined by the relative rates of H⁺ consumed during photosynthesis and H⁺ generated during calcification. In a cell taking up CO₂, the H⁺ budget is determined primarily by calcification, as 2 H⁺ are produced for each molecule of CaCO₃ produced and H⁺ are no longer consumed during photosynthesis. In both scenarios, excess H⁺ may be removed from the cell by H⁺ transporters in the plasma membrane, such as voltage-gated H⁺ channels (H_v). Coccolithophores take up both HCO₃⁻ and CO₂ across the plasma membrane, with increasing proportions of DIC taken up as CO₂ as seawater CO₂ increases (34). (B) Growth rate of C. braarudii cells acclimated to different seawater pH. n = 3 replicates per treatment; line represents polynomial fit to mean. (C) Cellular production of POC through photosynthesis and PIC through calcification. The optima for both processes are close to the control conditions (pH 8.15). (D) As a consequence of the unequal changes in cellular POC and PIC production across the applied pH values, cellular PIC/POC ratios are minimal at pH 7.55 (∼1.0) and maximal at pH 8.45 (∼1.8). (E) Calculated net H⁺ budgets under the different pH regimes, based on rates of photosynthesis and calcification shown in C (see Materials and Methods). The concentration of CO₂ in seawater is also shown (dashed line). Estimates are shown for cells using taking up only HCO₃⁻ or only CO₂. As C. braarudii cells will likely take up a mixture of both DIC species, with a shift toward greater CO₂ usage at elevated CO₂, the shaded area represents the potential range of H⁺ production. Regardless of DIC species used C. braarudii produces excess H⁺ at all applied pH values, but H⁺ production is much lower at pH 7.55 due to the decrease in calcification.In this study we set out to better understand the cellular mechanisms underlying the sensitivity of coccolithophore calcification to lower pH. We subjected the heavily calcified species C. braarudii, which is commonly found in temperate upwelling regions (35, 36), to conditions that reflect the range of pH values it may experience in current and future oceans. We show that acclimation to low pH leads to loss of H⁺ channel function and disruption of cellular pH regulation in C. braarudii. These effects are coincident with very specific defects in coccolith morphology that can be reproduced by direct inhibition of H⁺ channels. We conclude that H⁺ efflux through H⁺ channels is essential for maintaining both calcification rate and coccolith morphology. By providing a mechanistic insight into pH regulation during the calcification process, our results indicate that disruption of coccolithophore calcification in a future acidified ocean is likely to be most severe in heavily calcified species.     

活性炭表面酸化改性对催化聚丙烯成炭的影响

通过硝酸氧化处理对椰壳类活性炭(AC)进行酸化改性,研究酸化条件(温度、时间、浓度)对AC酸值的影响,并考察不同酸值的AC对PP(聚丙烯)/NiO/AC复合材料成炭的影响。采用比表面积及孔径分析仪考察改性活性炭的比表面积及孔结构;以Beohm滴定实验、X射线光电子能谱(XPS)表征改性AC表面含氧官能团种类及含量;用马弗炉、扫描电镜(SEM)考察不同酸值的AC和NiO协效催化聚丙烯成炭及成炭结构。实验结果表明:硝酸处理后,AC比表面积和孔结构均有所变化;酸化条件对AC表面酸性官能团的含量影响显著,改性后表面酸性官能团含量明显增加,酸性官能团主要为-COOH、-CO和-OH;AC表面酸性官能团的增多促进了聚丙烯自身成炭能力,改善了残炭结构。     

31P and 1H MRS of DB‐1 melanoma xenografts: lonidamine selectively decreases tumor intracellular pH and energy status and sensitizes tumors to melphalan

In vivo ³¹P MRS demonstrates that human melanoma xenografts in immunosuppressed mice treated with lonidamine (LND, 100 mg/kg intraperitoneally) exhibit a decrease in intracellular pH (pH_i) from 6.90 ± 0.05 to 6.33 ± 0.10 (p < 0.001), a slight decrease in extracellular pH (pH_e) from 7.00 ± 0.04 to 6.80 ± 0.07 (p > 0.05) and a monotonic decline in bioenergetics (nucleoside triphosphate/inorganic phosphate) of 66.8 ± 5.7% (p < 0.001) relative to the baseline level. Both bioenergetics and pH_i decreases were sustained for at least 3 h following LND treatment. Liver exhibited a transient intracellular acidification by 0.2 ± 0.1 pH units (p > 0.05) at 20 min post‐LND, with no significant change in pH_e and a small transient decrease in bioenergetics (32.9 ± 10.6%, p > 0.05) at 40 min post‐LND. No changes in pH_i or adenosine triphosphate/inorganic phosphate were detected in the brain (pH_i, bioenergetics; p > 0.1) or skeletal muscle (pH_i, pH_e, bioenergetics; p > 0.1) for at least 120 min post‐LND. Steady‐state tumor lactate monitored by ¹H MRS with a selective multiquantum pulse sequence with Hadamard localization increased approximately three‐fold (p = 0.009). Treatment with LND increased the systemic melanoma response to melphalan (LPAM; 7.5 mg/kg intravenously), producing a growth delay of 19.9 ± 2.0 days (tumor doubling time, 6.15 ± 0.31 days; log₁₀ cell kill, 0.975 ± 0.110; cell kill, 89.4 ± 2.2%) compared with LND alone of 1.1 ± 0.1 days and LPAM alone of 4.0 ± 0.0 days. The study demonstrates that the effects of LND on tumor pH_i and bioenergetics may sensitize melanoma to pH‐dependent therapeutics, such as chemotherapy with alkylating agents or hyperthermia. Copyright © 2012 John Wiley & Sons, Ltd.     

Acidification of stratum corneum prevents the progression from atopic dermatitis to respiratory allergy

The presence of congenitally impaired skin barrier followed by atopic dermatitis (AD) is an initial step in the atopic march. The maintenance of acidic pH in the stratum corneum (SC) has been suggested as a therapeutic or preventive strategy for barrier impairment caused by skin inflammation. To determine whether an AD murine model, flaky tail mice, with inherited filaggrin deficiency could develop airway inflammation by repeated topical application followed by nasal inhalation of house dust mite (HDM) antigen (defined as a novel “atopic march animal model”), and whether maintenance of an acidic SC environment by continuous application of acidic cream could interrupt the following atopic march. During the course of HDM treatment, acidic cream (pH2.8) or neutral cream (pH7.4) was applied to flaky tail mice twice daily. Repeated applications and inhalations of HDM to flaky tail mice induced AD skin lesions followed by respiratory allergies. Maintenance of SC acidity inhibited the occurrence of respiratory allergic inflammation as well as AD‐like skin lesions. Collectively, a novel atopic march model could be developed by repeated epicutaneous and nasal applications of HDM to flaky tail mice, and that the acidification of SC could prevent the atopic march from AD to respiratory allergy.     

Effects of pH and Nutrients (Nitrogen) on Growth and Toxin Profile of the Ciguatera-Causing Dinoflagellate Gambierdiscus polynesiensis (Dinophyceae)

Ciguatera poisoning is a foodborne disease caused by the consumption of seafood contaminated with ciguatoxins (CTXs) produced by dinoflagellates in the genera Gambierdiscus and Fukuyoa. Ciguatera outbreaks are expected to increase worldwide with global change, in particular as a function of its main drivers, including changes in sea surface temperature, acidification, and coastal eutrophication. In French Polynesia, G. polynesiensis is regarded as the dominant source of CTXs entering the food web. The effects of pH (8.4, 8.2, and 7.9), Nitrogen:Phosphorus ratios (24N:1P vs. 48N:1P), and nitrogen source (nitrates vs. urea) on growth rate, biomass, CTX levels, and profiles were examined in four clones of G. polynesiensis at different culture age (D10, D21, and D30). Results highlight a decrease in growth rate and cellular biomass at low pH when urea is used as a N source. No significant effect of pH, N:P ratio, and N source on the overall CTX content was observed. Up to ten distinct analogs of Pacific ciguatoxins (P-CTXs) could be detected by liquid chromatography-tandem mass spectrometry (LC-MS/MS) in clone NHA4 grown in urea, at D21. Amounts of more oxidized P-CTX analogs also increased under the lowest pH condition. These data provide interesting leads for the custom production of CTX standards.     

From the Cover: Dynamic patterns and ecological impacts of declining ocean pH in a high-resolution multi-year dataset

Increasing global concentrations of atmospheric CO₂ are predicted to decrease ocean pH, with potentially severe impacts on marine food webs, but empirical data documenting ocean pH over time are limited. In a high-resolution dataset spanning 8 years, pH at a north-temperate coastal site declined with increasing atmospheric CO₂ levels and varied substantially in response to biological processes and physical conditions that fluctuate over multiple time scales. Applying a method to link environmental change to species dynamics via multispecies Markov chain models reveals strong links between in situ benthic species dynamics and variation in ocean pH, with calcareous species generally performing more poorly than noncalcareous species in years with low pH. The models project the long-term consequences of these dynamic changes, which predict substantial shifts in the species dominating the habitat as a consequence of both direct effects of reduced calcification and indirect effects arising from the web of species interactions. Our results indicate that pH decline is proceeding at a more rapid rate than previously predicted in some areas, and that this decline has ecological consequences for near shore benthic ecosystems.     

酸化中药液熏洗联合超短波对膝骨性关节炎患者血清hs-CRP的影响

目的：观察酸化中药液熏洗联合超短波治疗膝骨性关节炎对患者血清超敏C反应蛋白（hs-CRP）的影响。方法150例膝骨性关节炎患者随机分为三组（n=50）：A组采用酸化中药液熏洗结合短波治疗;B组采用酸化中药液熏洗治疗;C组采用超短波治疗。三组患者分别在治疗后2周、1月、3月采用免疫荧光法检测患者血清hs-CRP水平。结果三组治疗前血清hs-CRP差异无统计学意义（F=3.73,P＞0.05）;A组患者治疗后2周、1月、3月与治疗前血清hs-CRP比较,差异有统计学意义（t分别=-17.84、-16.12、-9.76,P均＜0.05）;B组患者治疗后2周、1月、3月与治疗前血清hs-CRP比较,差异有统计学意义（t分别=-13.88、-12.40、-2.73,P均＜0.05）;C组患者治疗后2周、1月与治疗前血清hs-CRP比较,差异有统计学意义（t分别=-7.02、-3.47,P均＜0.05）;治疗后2周、1月、3月三组间血清CRP下降水平比较,差异有统计学意义（F分别=24.03、42.71、58.41,P均＜0.05）。结论对于膝骨性关节炎的治疗,酸化中药液熏洗结合短波治疗能持续有效降低血清hs-CRP水平。