Elevated carbon dioxide affects behavioural lateralization in a coral reef fish

Elevated carbon dioxide (CO(2)) has recently been shown to affect chemosensory and auditory behaviour, and activity levels of larval reef fishes, increasing their risk of predation. However, the mechanisms underlying these changes are unknown. Behavioural lateralization is an expression of brain functional asymmetries, and thus provides a unique test of the hypothesis that elevated CO(2) affects brain function in larval fishes. We tested the effect of near-future CO(2) concentrations (880 μatm) on behavioural lateralization in the reef fish, Neopomacentrus azysron. Individuals exposed to current-day or elevated CO(2) were observed in a detour test where they made repeated decisions about turning left or right. No preference for right or left turns was observed at the population level. However, individual control fish turned either left or right with greater frequency than expected by chance. Exposure to elevated-CO(2) disrupted individual lateralization, with values that were not different from a random expectation. These results provide compelling evidence that elevated CO(2) directly affects brain function in larval fishes. Given that lateralization enhances performance in a number of cognitive tasks and anti-predator behaviours, it is possible that a loss of lateralization could increase the vulnerability of larval fishes to predation in a future high-CO(2) ocean.     

Elevated pCO2 increases sperm limitation and risk of polyspermy in the red sea urchin Strongylocentrotus franciscanus

Anthropogenic carbon dioxide (CO₂) emissions and the resultant acidification of surface ocean waters are predicted to have far‐reaching consequences for biological processes in the marine environment. For example, because changes in pH and pCO₂ can alter sperm performance, ocean acidification may be accompanied by reductions in the success of fertilization in marine broadcast spawners. Several studies have attempted to determine the effects of elevated pCO₂ on marine invertebrate fertilization success, albeit with differing results. These conflicts may stem from the use of inappropriate sperm–egg contact times and, in several cases, the lack of measurements over a range of sperm concentrations extending from sperm‐limited conditions to polyspermy scenarios. In our study, we used biologically realistic sperm–egg contact times and a full range of sperm concentrations to assess the effect of elevated pCO₂ on fertilization in the broadcast spawning sea urchin, Strongylocentrotus franciscanus. Fertilization experiments were carried out in seawater bubbled with CO₂ to 400 (control), 800, and 1800 ppm. Using a fertilization kinetics model, we estimate that elevated pCO₂ levels both increased sperm limitation and reduced the efficiency of fast blocks to polyspermy. Thus, elevated pCO₂ decreased the range of sperm concentrations over which high fertilization success was likely. Given the inherent difficulties in achieving high fertilization success in broadcast spawners, raised pCO₂ levels are likely to exacerbate low fertilization success in low‐density populations or in areas with high water turbulence.     

On the potential for ocean acidification to be a general cause of ancient reef crises

Anthropogenic rise in the carbon dioxide concentration in the atmosphere leads to global warming and acidification of the oceans. Ocean acidification (OA) is harmful to many organisms but especially to those that build massive skeletons of calcium carbonate, such as reef corals. Here, we test the recent suggestion that OA leads not only to declining calcification of reef corals and reduced growth rates of reefs but may also have been a trigger of ancient reef crises and mass extinctions in the sea. We analyse the fossil record of biogenic reefs and marine organisms to (1) assess the timing and intensity of ancient reef crises, (2) check which reef crises were concurrent with inferred pulses of carbon dioxide concentrations and (3) evaluate the correlation between reef crises and mass extinctions and their selectivity in terms of inferred physiological buffering. We conclude that four of five global metazoan reef crises in the last 500 Myr were probably at least partially governed by OA and rapid global warming. However, only two of the big five mass extinctions show geological evidence of OA.     

Behavioural asymmetry affects escape performance in a teleost fish

Escape performance is fundamental for survival in fish and most other animals. While previous work has shown that both intrinsic (e.g. size, shape) and extrinsic (e.g. temperature, hypoxia) factors can affect escape performance, the possibility that behavioural asymmetry may affect timing and locomotor performance in startled fish is largely unexplored. Numerous studies have found a relationship between brain lateralization and performance in several cognitive tasks. Here, we tested the hypothesis that behavioural lateralization may affect escape performance in a teleost, the shiner perch Cymatogaster aggregata. Escape responses were elicited by mechanical stimulation and recorded using high-speed video (250 Hz). A number of performance variables were analysed, including directionality, escape latency, turning rate and distance travelled within a fixed time. A lateralization index was obtained by testing the turning preference of each subject in a detour test. While lateralization had no effect on escape directionality, strongly lateralized fish showed higher escape reactivity, i.e. shorter latencies, which were associated with higher turning rates and longer distances travelled. Therefore, lateralization is likely to result in superior ability to escape from predator attacks, since previous work has shown that escape timing, turning rate and distance travelled are among the main determinants of escape success.     

Acclimation to predicted ocean warming through developmental plasticity in a tropical reef fish

Determining the capacity of organisms to acclimate and adapt to increased temperatures is key to understand how populations and communities will respond to global warming. Although there is evidence that elevated water temperature affects metabolism, growth and condition of tropical marine fish, it is unknown whether they have the potential to acclimate, given adequate time. We reared the tropical reef fish Acanthochromis polyacanthus through its entire life cycle at present day and elevated (+1.5 and+3.0 °C) water temperatures to test its ability to thermally acclimate to ocean temperatures predicted to occur over the next 50–100 years. Fish reared at 3.0 °C greater than the present day average reduced their resting oxygen consumption (RMR) during summer compared with fish reared at present day temperatures and tested at the elevated temperature. The reduction in RMR of up to 69 mg O₂ kg^?1 h^?1 in acclimated fish could represent a significant benefit to daily energy expenditure. In contrast, there was no acclimation to summer temperatures exhibited by fish reared at 1.5 °C above present day temperatures. Fish acclimated to +3.0 °C were smaller and in poorer condition than fish reared at present day temperatures, suggesting that even with acclimation there will be significant consequences for future populations of tropical fishes caused by global warming.     

Parental condition affects early life-history of a coral reef fish

Parents can exert a range of non-genetic effects on the growth and survival of their offspring. In particular, parents may modify the size or condition of their offspring depending on the amount of energy they have available for reproduction. In this study, the body condition of breeding pairs of the coral reef fish Acanthochromis polyacanthus was experimentally manipulated to test the effects of parental condition on reproductive output and offspring life history traits. Parents in good condition commenced breeding earlier, had higher reproductive output, and their eggs exhibited increased survival during embryogenesis, compared to parents in poorer condition. Increased reproductive output was attained through more reproductive bouts over the breeding season that contained both a greater number and an increased size of eggs. The offspring from parents in good condition were larger at hatching, with larger yolk reserves and increased survival on endogenous reserves. Larger size is expected to provide benefits to offspring through reduced susceptibility to size-selective mortality. The range of offspring characteristics modified by parental condition could result in a greater proportion of offspring from good condition parents recruiting to the population.     

Effects of ocean acidification on the early life history of a tropical marine fish

Little is known about how fishes and other non-calcifying marine organisms will respond to the increased levels of dissolved CO₂ and reduced sea water pH that are predicted to occur over the coming century. We reared eggs and larvae of the orange clownfish, Amphiprion percula, in sea water simulating a range of ocean acidification scenarios for the next 50–100 years (current day, 550, 750 and 1030 ppm atmospheric CO₂). CO₂ acidification had no detectable effect on embryonic duration, egg survival and size at hatching. In contrast, CO₂ acidification tended to increase the growth rate of larvae. By the time of settlement (11 days post-hatching), larvae from some parental pairs were 15 to 18 per cent longer and 47 to 52 per cent heavier in acidified water compared with controls. Larvae from other parents were unaffected by CO₂ acidification. Elevated CO₂ and reduced pH had no effect on the maximum swimming speed of settlement-stage larvae. There was, however, a weak positive relationship between length and swimming speed. Large size is usually considered to be advantageous for larvae and newly settled juveniles. Consequently, these results suggest that levels of ocean acidification likely to be experienced in the near future might not, in isolation, significantly disadvantage the growth and performance of larvae from benthic-spawning marine fishes.     

Possible effects of rising C02 on climate

Abstract Two factors will determine the rate at which CO₂ levels in the atmosphere increase in the future: the rate of input to the atmosphere, primarily from fossil fuel burning, and the way in which this CO₂ is partitioned between atmosphere, ocean and biosphere. A brief review is given of the current state of knowledge of these aspects of the CO₂ issue prior to a discussion of the changes in climate that might be expected from increased levels of CO₂, whenever these might occur. The basis of climate modelling upon which our expectations rest is explained, indicating the nature of the uncertainty that currently exists in the model results. While some of the gross features of the likely climatic change seem reasonably well established qualitatively, considerable model development will be needed before reliable information on the likely regional effects is forthcoming. Observations have yet to confirm the occurrence of temperature change attributable to CO₂ increases. Nevertheless, the possibility exists of a change in climate during the coming century that may be substantial relative to past experience. Although direct measures to control CO₂ emissions would certainly be premature, long-term planning of infrastructures, closely tuned to present climatic conditions, should ensure their robustness in the face of the uncertain climatic changes that may lie ahead.     

Unshelled abalone and corrupted urchins: development of marine calcifiers in a changing ocean

The most fragile skeletons produced by benthic marine calcifiers are those that larvae and juveniles make to support their bodies. Ocean warming, acidification, decreased carbonate saturation and their interactive effects are likely to impair skeletogenesis. Failure to produce skeleton in a changing ocean has negative implications for a diversity of marine species. We examined the interactive effects of warming and acidification on an abalone (Haliotis coccoradiata) and a sea urchin (Heliocidaris erythrogramma) reared from fertilization in temperature and pH/pCO(2) treatments in a climatically and regionally relevant setting. Exposure of ectodermal (abalone) and mesodermal (echinoid) calcifying systems to warming (+2°C to 4°C) and acidification (pH 7.6-7.8) resulted in unshelled larvae and abnormal juveniles. Haliotis development was most sensitive with no interaction between stressors. For Heliocidaris, the percentage of normal juveniles decreased in response to both stressors, although a +2°C warming diminished the negative effect of low pH. The number of spines produced decreased with increasing acidification/pCO(2), and the interactive effect between stressors indicated that a +2°C warming reduced the negative effects of low pH. At +4°C, the developmental thermal tolerance was breached. Our results show that projected near-future climate change will have deleterious effects on development with differences in vulnerability in the two species.     

Acclimation response of spring wheat in a free-air CO2 enrichment (FACE) atmosphere with variable soil nitrogen regimes. 1. Leaf position and phenology determine acclimation response

We have examined the photosynthetic acclimation of wheat leaves grown at an elevated CO₂ concentration, and ample and limiting N supplies, within a field experiment using free-air CO₂ enrichment (FACE). To understand how leaf age and developmental stage affected any acclimation response, measurements were made on a vertical profile of leaves every week from tillering until maturity. The response of assimilation (A) to internal CO₂ concentration (C_i) was used to estimate the in vivo carboxylation capacity (Vc_max) and maximum rate of ribulose-1,5-bisphosphate limited photosynthesis (A _sat). The total activity of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco), and leaf content of Rubisco and the Light Harvesting Chlorophyll a/b protein associated with Photosystem II (LHC II), were determined. Elevated CO₂ did not alter Vc_max in the flag leaf at either low or high N. In the older shaded leaves lower in the canopy, acclimatory decline in Vc_max and A _sat was observed, and was found to correlate with reduced Rubisco activity and content. The dependency of acclimation on N supply was different at each developmental stage. With adequate N supply, acclimation to elevated CO₂ was also accompanied by an increased LHC II/Rubisco ratio. At low N supply, contents of Rubisco and LHC II were reduced in all leaves, although an increased LHC II/Rubisco ratio under elevated CO₂ was still observed. These results underscore the importance of leaf position, leaf age and crop developmental stage in understanding the acclimation of photosynthesis to elevated CO₂ and nutrient stress. This revised version was published online in June 2006 with corrections to the Cover Date.     

Ocean warming and acidification have complex interactive effects on the dynamics of a marine fungal disease

Diseases threaten the structure and function of marine ecosystems and are contributing to the global decline of coral reefs. We currently lack an understanding of how climate change stressors, such as ocean acidification (OA) and warming, may simultaneously affect coral reef disease dynamics, particularly diseases threatening key reef-building organisms, for example crustose coralline algae (CCA). Here, we use coralline fungal disease (CFD), a previously described CCA disease from the Pacific, to examine these simultaneous effects using both field observations and experimental manipulations. We identify the associated fungus as belonging to the subphylum Ustilaginomycetes and show linear lesion expansion rates on individual hosts can reach 6.5 mm per day. Further, we demonstrate for the first time, to our knowledge, that ocean-warming events could increase the frequency of CFD outbreaks on coral reefs, but that OA-induced lowering of pH may ameliorate outbreaks by slowing lesion expansion rates on individual hosts. Lowered pH may still reduce overall host survivorship, however, by reducing calcification and facilitating fungal bio-erosion. Such complex, interactive effects between simultaneous extrinsic environmental stressors on disease dynamics are important to consider if we are to accurately predict the response of coral reef communities to future climate change.     

Acclimation of Russian forests to recent changes in climate

Assessments made over the past few decades have suggested that boreal forests may act as a sink for atmospheric carbon dioxide. However, the fate of the newly accumulated carbon in the living forest biomass is not well understood, and the estimates of carbon sinks vary greatly from one assessment to another. Analysis of remote sensing data has indicated that the carbon sinks in the Russian forests are larger than what has been estimated from forest inventories. In this study, we show that over the past four decades, the allometric relationships among various plant parts have changed in the Russian forests. To this end, we employ two approaches: (1) analysis of the database, which contains 3196 sample plots; and (2) application of developed models to forest inventory data. Within the forests as a whole, when assessed at the continental scale, we detect a pronounced increase in the share of green parts (leaves and needles). However, there is a large geographical variation. The shift has been largest within the European Russia, where summer temperatures and precipitation have increased. In the Northern Taiga of Siberia, where the climate has become warmer but drier, the fraction of the green parts has decreased while the fractions of aboveground wood and roots have increased. These changes are consistent with experiments and mathematical models that predict a shift of carbon allocation to transpiring foliage with increasing temperature and lower allocation with increasing soil drought. In light of this, our results are a possible demonstration of the acclimation of trees to ongoing warming and changes in the surface water balance. Independent of the nature of the observed changes in allometric ratios, the increase in the share of green parts may have caused a misinterpretation of the satellite data and a systematic overestimation by remote sensing methods of the carbon sink for living biomass of the Russian forest.     

Adaptation and acclimatization to ocean acidification in marine ectotherms: an in situ transplant experiment with polychaetes at a shallow CO2 vent system

Metabolic rate determines the physiological and life-history performances of ectotherms. Thus, the extent to which such rates are sensitive and plastic to environmental perturbation is central to an organism''s ability to function in a changing environment. Little is known of long-term metabolic plasticity and potential for metabolic adaptation in marine ectotherms exposed to elevated pCO₂. Consequently, we carried out a series of in situ transplant experiments using a number of tolerant and sensitive polychaete species living around a natural CO₂ vent system. Here, we show that a marine metazoan (i.e. Platynereis dumerilii) was able to adapt to chronic and elevated levels of pCO₂. The vent population of P. dumerilii was physiologically and genetically different from nearby populations that experience low pCO₂, as well as smaller in body size. By contrast, different populations of Amphiglena mediterranea showed marked physiological plasticity indicating that adaptation or acclimatization are both viable strategies for the successful colonization of elevated pCO₂ environments. In addition, sensitive species showed either a reduced or increased metabolism when exposed acutely to elevated pCO₂. Our findings may help explain, from a metabolic perspective, the occurrence of past mass extinction, as well as shed light on alternative pathways of resilience in species facing ongoing ocean acidification.     

Ocean acidification increases the vulnerability of native oysters to predation by invasive snails

There is growing concern that global environmental change might exacerbate the ecological impacts of invasive species by increasing their per capita effects on native species. However, the mechanisms underlying such shifts in interaction strength are poorly understood. Here, we test whether ocean acidification, driven by elevated seawater pCO₂, increases the susceptibility of native Olympia oysters to predation by invasive snails. Oysters raised under elevated pCO₂ experienced a 20% increase in drilling predation. When presented alongside control oysters in a choice experiment, 48% more high-CO₂ oysters were consumed. The invasive snails were tolerant of elevated CO₂ with no change in feeding behaviour. Oysters raised under acidified conditions did not have thinner shells, but were 29–40% smaller than control oysters, and these smaller individuals were consumed at disproportionately greater rates. Reduction in prey size is a common response to environmental stress that may drive increasing per capita effects of stress-tolerant invasive predators.