A decade of climate change experiments on marine organisms: procedures,patterns and problems

The first decade of the new millennium saw a flurry of experiments to establish a mechanistic understanding of how climate change might transform the global biota, including marine organisms. However, the biophysical properties of the marine environment impose challenges to experiments, which can weaken their inference space. To facilitate strengthening the experimental evidence for possible ecological consequences of climate change, we reviewed the physical, biological and procedural scope of 110 marine climate change experiments published between 2000 and 2009. We found that 65% of these experiments only tested a single climate change factor (warming or acidification), 54% targeted temperate organisms, 58% were restricted to a single species and 73% to benthic invertebrates. In addition, 49% of the reviewed experiments had issues with the experimental design, principally related to replication of the main test‐factors (temperature or pH), and only 11% included field assessments of processes or associated patterns. Guiding future research by this inventory of current strengths and weaknesses will expand the overall inference space of marine climate change experiments. Specifically, increased effort is required in five areas: (i) the combined effects of concurrent climate and non‐climate stressors; (ii) responses of a broader range of species, particularly from tropical and polar regions as well as primary producers, pelagic invertebrates, and fish; (iii) species interactions and responses of species assemblages, (iv) reducing pseudo‐replication in controlled experiments; and (v) increasing realism in experiments through broad‐scale observations and field experiments. Attention in these areas will improve the generality and accuracy of our understanding of climate change as a driver of biological change in marine ecosystems.     

The impacts of climate change in coastal marine systems

Anthropogenically induced global climate change has profound implications for marine ecosystems and the economic and social systems that depend upon them. The relationship between temperature and individual performance is reasonably well understood, and much climate-related research has focused on potential shifts in distribution and abundance driven directly by temperature. However, recent work has revealed that both abiotic changes and biological responses in the ocean will be substantially more complex. For example, changes in ocean chemistry may be more important than changes in temperature for the performance and survival of many organisms. Ocean circulation, which drives larval transport, will also change, with important consequences for population dynamics. Furthermore, climatic impacts on one or a few 'leverage species' may result in sweeping community-level changes. Finally, synergistic effects between climate and other anthropogenic variables, particularly fishing pressure, will likely exacerbate climate-induced changes. Efforts to manage and conserve living marine systems in the face of climate change will require improvements to the existing predictive framework. Key directions for future research include identifying key demographic transitions that influence population dynamics, predicting changes in the community-level impacts of ecologically dominant species, incorporating populations' ability to evolve (adapt), and understanding the scales over which climate will change and living systems will respond.     

Mixed-conifer understory response to climate change, nitrogen, and fire

California's Sierra Nevada mountains are predicted to experience greater variation in annual precipitation according to climate change models, while nitrogen deposition from pollution continues to increase. These changes may significantly affect understory communities and fuels in forests where managers are attempting to restore historic conditions after a century of altered fire regimes. The objective of this research was to experimentally test the effects of increasing and decreasing snowpack depth, increasing nitrogen, and applying prescribed fire to mixed-conifer forest understories at two sites in the central and southern Sierra Nevada. Understory response to treatments significantly differed between sites with herb biomass increasing in shrub-dominated communities when snowpack was reduced. Fire was a more important factor in post-treatment species richness and cover than either snowpack addition or reduction. Nitrogen additions unexpectedly increased herbaceous species richness. These varied findings indicate that modeling future climatic influences on biodiversity may be more difficult than additive prediction based on increasing the ecosystem's two limiting growth resources. Increasing snowpack and nitrogen resulted in increased shrub biomass production at both sites and increased herb production at the southern site. This additional understory biomass has the potential to increase fuel connectivity in patchy Sierran mixed-conifer forests, increasing fire severity and size.     

The potential impacts of global climate change on marine protected areas

The potential effects of global climate changeon marine protected areas do not appear to havebeen addressed in the literature. This paperexamines the literature on protected areas,conservation biology, marine ecology,oceanography, and climate change, and reviewssome of the relevant differences between marineand terrestrial environments. Frameworks andclassifications systems used in protected areadesign are discussed. Finally, a frameworkthat summarizes some of the importantoceanographic processes and their links to thefood chain are reviewed. Species abundance anddistribution are expected to change as a resultof global climate change, potentiallycompromising the efficacy of marine protectedareas as biodiversity conservation tools. Thisreview suggests the need for: furtherinterdisciplinary research and the use oflinked models; an increase in marine protectedareas for biodiversity conservation and asresearch sites for teasing apart fishingeffects from climate effects; a temporallyresponsive approach to siting new marineprotected areas, shifting their locations ifnecessary; and large-scale ecosystem/integratedmanagement approaches to address the competinguses of the oceans and boundary-less threatssuch as global climate change and pollution.     

The potential impacts of global climate change on marine protected areas

Reviews in Fish Biology and Fisheries - The potential effects of global climate changeon marine protected areas do not appear to havebeen addressed in the literature. This paperexamines the...     

Projected marine climate change: effects on copepod oxidative status and reproduction

Zooplankton are an important link between primary producers and fish. Therefore, it is crucial to address their responses when predicting effects of climate change on pelagic ecosystems. For realistic community‐level predictions, several biotic and abiotic climate‐related variables should be examined in combination. We studied the combined effects of ocean acidification and global warming predicted for year 2100 with toxic cyanobacteria on the calanoid copepod, Acartia bifilosa. Acidification together with higher temperature reduced copepod antioxidant capacity. Higher temperature also decreased egg viability, nauplii development, and oxidative status. Exposure to cyanobacteria and its toxin had a negative effect on egg production but, a positive effect on oxidative status and egg viability, giving no net effects on viable egg production. Additionally, nauplii development was enhanced by the presence of cyanobacteria, which partially alleviated the otherwise negative effects of increased temperature and decreased pH on the copepod recruitment. The interactive effects of temperature, acidification, and cyanobacteria on copepods highlight the importance of testing combined effects of climate‐related factors when predicting biological responses.     

Using fuzzy logic to determine the vulnerability of marine species to climate change

Marine species are being impacted by climate change and ocean acidification, although their level of vulnerability varies due to differences in species' sensitivity, adaptive capacity and exposure to climate hazards. Due to limited data on the biological and ecological attributes of many marine species, as well as inherent uncertainties in the assessment process, climate change vulnerability assessments in the marine environment frequently focus on a limited number of taxa or geographic ranges. As climate change is already impacting marine biodiversity and fisheries, there is an urgent need to expand vulnerability assessment to cover a large number of species and areas. Here, we develop a modelling approach to synthesize data on species‐specific estimates of exposure, and ecological and biological traits to undertake an assessment of vulnerability (sensitivity and adaptive capacity) and risk of impacts (combining exposure to hazards and vulnerability) of climate change (including ocean acidification) for global marine fishes and invertebrates. We use a fuzzy logic approach to accommodate the variability in data availability and uncertainties associated with inferring vulnerability levels from climate projections and species' traits. Applying the approach to estimate the relative vulnerability and risk of impacts of climate change in 1074 exploited marine species globally, we estimated their index of vulnerability and risk of impacts to be on average 52 ± 19 SD and 66 ± 11 SD, scaling from 1 to 100, with 100 being the most vulnerable and highest risk, respectively, under the ‘business‐as‐usual' greenhouse gas emission scenario (Representative Concentration Pathway 8.5). We identified 157 species to be highly vulnerable while 294 species are identified as being at high risk of impacts. Species that are most vulnerable tend to be large‐bodied endemic species. This study suggests that the fuzzy logic framework can help estimate climate vulnerabilities and risks of exploited marine species using publicly and readily available information.     

Investigating the potential impacts of climate change on a marine turtle population

Recent increases in global temperatures have affected the phenology and survival of many species of plants and animals. We investigated a case study of the effects of potential climate change on a thermally sensitive species, the loggerhead sea turtle, at a breeding location at the northerly extent of the range of regular nesting in the United States. In addition to the physical limits imposed by temperature on this ectothermic species, sea turtle primary sex ratio is determined by the temperature experienced by eggs during the middle third of incubation. We recorded sand temperatures and used historical air temperatures (ATs) at Bald Head Island, NC, to examine past and predict future sex ratios under scenarios of warming. There were no significant temporal trends in primary sex ratio evident in recent years and estimated mean annual sex ratio was 58% female. Similarly, there were no temporal trends in phenology but earlier nesting and longer nesting seasons were correlated with warmer sea surface temperature. We modelled the effects of incremental increases in mean AT of up to 7.5°C, the maximum predicted increase under modelled scenarios, which would lead to 100% female hatchling production and lethally high incubation temperatures, causing reduction in hatchling production. Populations of turtles in more southern parts of the United States are currently highly female biased and are likely to become ultra‐biased with as little as 1°C of warming and experience extreme levels of mortality if warming exceeds 3°C. The lack of a demonstrable increase in AT in North Carolina in recent decades coupled with primary sex ratios that are not highly biased means that the male offspring from North Carolina could play an increasingly important role in the future viability of the loggerhead turtle in the Western Atlantic.     

Transferring soils from high- to low-elevation forests increases nitrogen cycling rates: climate change implications

We assessed the potential impact of global warming resulting from a doubling of preindustrial atmospheric CO₂ on soil net N transformations by transferring intact soil cores (0–15 cm) from a high-elevation old-growth forest to a forest about 800 m lower in elevation in the central Oregon Cascade Mountains, USA. The lower elevation site had mean annual air and soil (10-cm mineral soil depth) temperatures about 2.4 and 3.9 °C higher than the high-elevation site, respectively. Annual rates of soil net N mineralization and nitrification more than doubled in soil transferred to the low-elevation site (17.2–36.0 kg N ha^–1 and 5.0–10.7 kg NO₃^––N ha^–1, respectively). Leaching of inorganic N from the surface soil (in the absence of plant uptake) also increased. The reciprocal treatment (transferring soil cores from the low- to the high-elevation site) resulted in decreases of about 70, 80, and 65% in annual rates of net N mineralization, nitrification, and inorganic N leaching, respectively. Laboratory incubations of soils under conditions of similar temperature and soil water potential suggest that the quality of soil organic matter is higher at the high-elevation site. Similar in situ rates of soil net N transformations between the two sites occurred because the lower temperature counteracts the effects of greater substrate quantity and quality at the high elevation site. Our results support the hypothesis that high-elevation, old-growth forest soils in the central Cascades have higher C and N storage than their low-elevation analogues primarily because low temperatures limit net C and N mineralization rates at higher elevations.     

Transferring soils from high- to low-elevation forests increases nitrogen cycling rates: climate change implications

It is well recognized that photosynthesis of C3 plants is highly responsive to CO₂ concentration. However, in natural ecosystems, plants are subject to a range of feed-back effects that can interact with increased photosynthetic carbon gain in different ways so that it is not clear to what extent increased photosynthesis will translate into increased growth. To assess the probable growth response of nutrient-limited forests to increasing CO₂ concentration, we use a previously developed modelling framework and apply it under conditions where the supply of nutrients is affected by a range of different factors. Our analysis indicates that forest growth is likely to be highly stimulated by increasing CO₂ concentration in forests with high fertility, in forests with nitrogen fixing plants, in those subject to fire or where nitrogen in wood is effectively removed from the biologically active cycle either through physical removal of stems in harvesting or through continued stem growth over long time periods. Forest growth is likely to be stimulated by CO₂ concentration in both phosphorus- and sulphur-limited forests provided nutrients in heartwood of trees are removed from the active nutrient cycle. Without this removal from the cycling system, however, sulphur-limited forests should show little response to increasing CO₂. In phosphorus-limited forests without phosphorus removal, the response to increasing CO₂ depends further on the equilibration state of the large pool of unavailable secondary phosphorus. Considered over periods of centuries during which the secondary pool has equilibrated, growth of phosphorus-limited forests is likely to be only weakly stimulated by increasing CO₂ concentration. However, over shorter periods, increasing CO₂ concentration should lead to a substantial increase in productivity. In general, it can be concluded that systems that are more open with respect to nutrient gains and losses are likely to be more responsive to increasing CO₂ concentration than systems where the amount of available nutrients is less variable. In more open systems, operation at a lower internal nutrient concentration as a result of increasing atmospheric CO₂ concentration can lead to reduced nutrient losses per unit carbon gain. Our analysis shows that the effect of increasing CO₂ on forest growth can differ substantially between forests due to interactions with a range of factors that affect nutrient supply. The response of a particular forest to increasing CO₂ concentration can only be predicted if the main factors controlling nutrient supply and growth in that forest are understood and incorporated into an assessment.     

The impact of humans on the nitrogen cycle,with focus on temperate arable agriculture

The 6 billion people alive today consume about 25 million tonnes of protein nitrogen each year, a requirement that could well increase to 40–45 million tonnes by 2050. Most of them ultimately depend on the Haber-Bosch process to fix the atmospheric N₂ needed to grow at least part of their protein and, over the earth as a whole, this dependency is likely to increase. Humans now fix some 160 million tonnes of nitrogen per year, of which 98 are fixed industrially by the Haber-Bosch process (83 for use as agricultural fertilizer, 15 for industry), 22 during combustion and the rest is fixed during the cultivation of leguminous crops and fodders. These 160 million tonnes have markedly increased the burden of combined nitrogen entering rivers, lakes and shallow seas, as well as increasing the input of NH₃, N₂O, NO and NO₂ to the atmosphere. Nitrogen fertilizers give large economic gains in modern farming systems and under favourable conditions can be used very efficiently. Losses of nitrogen occur from all systems of agriculture, with organic manures being particularly difficult to use efficiently. Although nitrate leaching has received much attention as an economic loss, a cause of eutrophication and a health hazard, gaseous emissions may eventually prove to be the most serious environmentally. Scientists working on the use and fate of nitrogen fertilizers must be careful, clear headed and vigilant in looking for unexpected side effects.     

微生物介导的碳氮循环过程对全球气候变化的响应

土壤是地球表层最为重要的碳库也是温室气体的源或汇。自工业革命以来,对土壤温室气体的容量、收支平衡和通量等已有较多研究和估算,但对关键过程及其源/汇的研究却十分有限。微生物是土壤碳氮转化的主要驱动者, 在生态系统碳氮循环过程中扮演重要的角色,对全球气候变化有着响应的响应、适应及反馈,然而其个体数量,群落结构和多样性如何与气候扰动相互关联、进而怎样影响生态系统过程的问题仍有待进一步探索。从微生物介导的碳氮循环过程入手,重点讨论微生物对气候变化包括温室气体(CO₂,CH₄,N₂O)增加、全球变暖、大气氮沉降等的响应和反馈,并由此提出削减温室气体排放的可能途径和今后发展的方向。     

Nitrogen source and pCO2 synergistically affect carbon allocation,growth and morphology of the coccolithophore Emiliania huxleyi: potential implications of ocean acidification for the carbon cycle

Coccolithophores are unicellular phytoplankton that produce calcium carbonate coccoliths as an exoskeleton. Emiliania huxleyi, the most abundant coccolithophore in the world's ocean, plays a major role in the global carbon cycle by regulating the exchange of CO₂ across the ocean‐atmosphere interface through photosynthesis and calcium carbonate precipitation. As CO₂ concentration is rising in the atmosphere, the ocean is acidifying and ammonium (NH₄⁺) concentration of future ocean water is expected to rise. The latter is attributed to increasing anthropogenic nitrogen (N) deposition, increasing rates of cyanobacterial N₂ fixation due to warmer and more stratified oceans, and decreased rates of nitrification due to ocean acidification. Thus, future global climate change will cause oceanic phytoplankton to experience changes in multiple environmental parameters including CO₂, pH, temperature and nitrogen source. This study reports on the combined effect of elevated pCO₂ and increased NH₄⁺ to nitrate (NO₃^?) ratio (NH₄⁺/NO₃^?) on E. huxleyi, maintained in continuous cultures for more than 200 generations under two pCO₂ levels and two different N sources. Herein, we show that NH₄⁺ assimilation under N‐replete conditions depresses calcification at both low and high pCO₂, alters coccolith morphology, and increases primary production. We observed that N source and pCO₂ synergistically drive growth rates, cell size, and the ratio of inorganic to organic carbon. These responses to N source suggest that, compared to increasing CO₂ alone, a greater disruption of the organic carbon pump could be expected in response to the combined effect of increased NH₄⁺/NO₃^? ratio and CO₂ level in the future acidified ocean. Additional experiments conducted under lower nutrient conditions are needed prior to extrapolating our findings to the global oceans. Nonetheless, our results emphasize the need to assess combined effects of multiple environmental parameters on phytoplankton biology to develop accurate predictions of phytoplankton responses to ocean acidification.     

Limitations of cross‐ and multigenerational plasticity for marine invertebrates faced with global climate change

Although cross generation (CGP) and multigenerational (MGP) plasticity have been identified as mechanisms of acclimation to global change, the weight of evidence indicates that parental conditioning over generations is not a panacea to rescue stress sensitivity in offspring. For many species, there were no benefits of parental conditioning. Even when improved performance was observed, this waned over time within a generation or across generations and fitness declined. CGP and MGP studies identified resilient species with stress tolerant genotypes in wild populations and selected family lines. Several bivalves possess favourable stress tolerance and phenotypically plastic traits potentially associated with genetic adaptation to life in habitats where they routinely experience temperature and/or acidification stress. These traits will be important to help ‘climate proof’ shellfish ventures. Species that are naturally stress tolerant and those that naturally experience a broad range of environmental conditions are good candidates to provide insights into the physiological and molecular mechanisms involved in CGP and MGP. It is challenging to conduct ecologically relevant global change experiments over the long times commensurate with the pace of changing climate. As a result, many studies present stressors in a shock‐type exposure at rates much faster than projected scenarios. With more gradual stressor introduction over longer experimental durations and in context with conditions species are currently acclimatized and/or adapted to, the outcomes for sensitive species might differ. We highlight the importance to understand primordial germ cell development and the timing of gametogenesis with respect to stressor exposure. Although multigenerational exposure to global change stressors currently appears limited as a universal tool to rescue species in the face of changing climate, natural proxies of future conditions (upwelling zones, CO₂ vents, naturally warm habitats) show that phenotypic adjustment and/or beneficial genetic selection is possible for some species, indicating complex plasticity–adaptation interactions.     

Dynamic larval dispersal can mediate the response of marine metapopulations to multiple climate change impacts

Climate change is having multiple impacts on marine species characterized by sedentary adult and pelagic larval phases, from increasing adult mortality to changes in larval duration and ocean currents. Recent studies have shown impacts of climate change on species persistence through direct effects on individual survival and development, but few have considered the indirect effects mediated by ocean currents and species traits such as pelagic larval duration. We used a density-dependent and stochastic metapopulation model to predict how changes in adult mortality and dynamic connectivity can affect marine metapopulation stability. We analyzed our model with connectivity data simulated from a biophysical ocean model of the northeast Pacific coast forced under current (1998–2007) and future (2068–2077) climate scenarios in combination with scenarios of increasing adult mortality and decreasing larval duration. Our results predict that changes of ocean currents and larval duration mediated by climate change interact in complex and opposing directions to shape local mortality and metapopulation connectivity with synergistic effects on regional metapopulation stability: while species with short larval duration are most sensitive to temperature-driven reduction in larval duration, the response of species with longer larval duration are mostly mediated by changes in both the mean and variance of larval connectivity driven by ocean currents. Our results emphasize the importance of considering the spatiotemporal structure of connectivity in order to predict how the multiple effects of climate change will impact marine populations.     

Global soil nitrogen cycle pattern and nitrogen enrichment effects: Tropical versus subtropical forests

Tropical and subtropical forest biomes are a main hotspot for the global nitrogen (N) cycle. Yet, our understanding of global soil N cycle patterns and drivers and their response to N deposition in these biomes remains elusive. By a meta-analysis of 2426-single and 161-paired observations from 89 published ¹⁵ N pool dilution and tracing studies, we found that gross N mineralization (GNM), immobilization of ammonium ($I_{{\mathrm{NH}}_4}$) and nitrate ($I_{{\mathrm{NO}}_3}$), and dissimilatory nitrate reduction to ammonium (DNRA) were significantly higher in tropical forests than in subtropical forests. Soil N cycle was conservative in tropical forests with ratios of gross nitrification (GN) to $I_{{\mathrm{NH}}_4}$ (GN/$I_{{\mathrm{NH}}_4}$) and of soil nitrate to ammonium (NO₃⁻/NH₄⁺) less than one, but was leaky in subtropical forests with GN/$I_{{\mathrm{NH}}_4}$ and NO₃⁻/NH₄⁺ higher than one. Soil NH₄⁺ dynamics were mainly controlled by soil substrate (e.g., total N), but climatic factors (e.g., precipitation and/or temperature) were more important in controlling soil NO₃⁻ dynamics. Soil texture played a role, as GNM and $I_{{\mathrm{NH}}_4}$ were positively correlated with silt and clay contents, while $I_{{\mathrm{NO}}_3}$ and DNRA were positively correlated with sand and clay contents, respectively. The soil N cycle was more sensitive to N deposition in tropical forests than in subtropical forests. Nitrogen deposition leads to a leaky N cycle in tropical forests, as evidenced by the increase in GN/$I_{{\mathrm{NH}}_4}$, NO₃⁻/NH₄⁺, and nitrous oxide emissions and the decrease in $I_{{\mathrm{NO}}_3}$ and DNRA, mainly due to the decrease in soil microbial biomass and pH. Dominant tree species can also influence soil N cycle pattern, which has changed from conservative in deciduous forests to leaky in coniferous forests. We provide global evidence that tropical, but not subtropical, forests are characterized by soil N dynamics sustaining N availability and that N deposition inhibits soil N retention and stimulates N losses in these biomes.     

全球降水格局变化下土壤氮循环研究进展

自然和人为因素导致全球降水格局发生改变,降水变化势必影响土壤氮循环,从而影响陆地生态系统生产力和多样性,然而不同降水变化类型对土壤氮循环的影响仍然缺乏足够的认识。因此,本文综合分析了全球和我国降水格局变化特征,简要介绍了6种降水格局变化下土壤氮循环的研究方法（长期降水固定观测、野外降水控制实验、自然降水梯度、室内培养、模型和遥感）,系统综述了3种降水变化类型（降水波动、干旱、干湿交替）,以及降水与温度、氮沉降等交互作用对土壤氮循环影响的研究进展与存在的问题,并展望了未来研究方向,为评估和预测未来降水变化对陆地生态系统功能的影响提供理论依据。