Bigfin reef squid demonstrate capacity for conditional discrimination and projected future carbon dioxide levels have no effect on learning capabilities

Anthropogenic carbon dioxide (CO2) emissions are being absorbed by the oceans, a process known as ocean acidification, and risks adversely affecting a variety of behaviours in a range of marine species, including inhibited learning in some fishes. However, the effects of elevated CO2 on learning in advanced invertebrates such as cephalopods are unknown. Any impacts to the learning abilities of cephalopods could have far-reaching consequences for their populations and the communities they inhabit. Cephalopods have some of the most advanced cognitive abilities among invertebrates and are one of the few invertebrate taxa in which conditional discrimination has been demonstrated, though the trait has not been demonstrated in any species of squid. Here, we tested for the first time the capacity for conditional discrimination in a squid species (Sepioteuthis lessoniana). Furthermore, we investigated the effects of projected future CO2 levels (1,084 mu atm) on conditional discrimination and learning more generally. A three-task experiment within a two-choice arena was used to test learning and conditional discrimination. Learning was measured by improvements in task completion in repeated trials over time and the number of trials required to pass each task. Squid exhibited significant learning capabilities, with an increase in correct choices over successive trials and a decrease in the number of trials needed to complete the successive tasks. Six of the 12 squid tested successfully passed all three tasks indicating a capacity for conditional discrimination in the species. Elevated CO2 had no effect on learning or on the capacity for conditional discrimination in squid. This study highlights the remarkable cognitive abilities of S. lessoniana, demonstrated by their capacity for conditional discrimination, and suggests that ocean acidification will not compromise learning abilities. However, other behavioural traits in the species have been shown to be altered at comparable elevated CO2 conditions. It is not clear why some ecologically important behaviours are altered by elevated CO2 whereas others are unaffected. Future research should focus on the physiological mechanism responsible for altered behaviours in squid at elevated CO2

Latitudinal trends in shell production cost from the tropics to the poles

The proportion of body mass devoted to skeleton in marine invertebrates decreases along latitudinal gradients from large proportions in the tropics to small proportions in polar regions. A historical hypothesis—that latitudinal differences in shell production costs explain these trends—remains untested. Using field-collected specimens spanning a 79°N to 68°S latitudinal gradient (16,300 km), we conducted a taxonomically controlled evaluation of energetic costs of shell production as a proportion of the total energy budget in mollusks. Shell production cost was fairly low across latitudes at <10% of the energy budget and predominately <5% in gastropods and <4% in bivalves. Throughout life, shell cost tended to be lower in tropical species and increased slightly toward the poles. However, shell cost also varied with life stage, with the greatest costs found in young tropical gastropods. Low shell production costs on the energy budget suggest that shell cost may play only a small role in influencing proportional skeleton size gradients across latitudes relative to other ecological factors, such as predation in present-day oceans. However, any increase in the cost of calcium carbonate (CaCO3) deposition, including from ocean acidification, may lead to a projected ~50 to 70% increase in the proportion of the total energy budget required for shell production for a doubling of the CaCO3 deposition cost. Changes in energy budget allocation to shell cost would likely alter ecological trade-offs between calcification and other drivers, such as predation, in marine ecosystems

Ocean acidification alters predator behaviour and reduces predation rate

Ocean acidification poses a range of threats to marine invertebrates; however, the emerging and likely widespread effects of rising carbon dioxide (CO₂) levels on marine invertebrate behaviour are still little understood. Here, we show that ocean acidification alters and impairs key ecological behaviours of the predatory cone snail Conus marmoreus. Projected near-future seawater CO₂ levels (975 µatm) increased activity in this coral reef molluscivore more than threefold (from less than 4 to more than 12 mm min⁻¹) and decreased the time spent buried to less than one-third when compared with the present-day control conditions (390 µatm). Despite increasing activity, elevated CO₂ reduced predation rate during predator–prey interactions with control-treated humpbacked conch, Gibberulus gibberulus gibbosus; 60% of control predators successfully captured and consumed their prey, compared with only 10% of elevated CO₂ predators. The alteration of key ecological behaviours of predatory invertebrates by near-future ocean acidification could have potentially far-reaching implications for predator–prey interactions and trophic dynamics in marine ecosystems. Combined evidence that the behaviours of both species in this predator–prey relationship are altered by elevated CO₂ suggests food web interactions and ecosystem structure will become increasingly difficult to predict as ocean acidification advances over coming decades

Toward a mechanistic understanding of marine invertebrate behavior at elevated CO2

Elevated carbon dioxide (CO2) levels can alter ecologically important behaviors in a range of marine invertebrate taxa; however, a clear mechanistic understanding of these behavioral changes is lacking. The majority of mechanistic research on the behavioral effects of elevated CO2 has been done in fish, focusing on disrupted functioning of the GABAA receptor (a ligand-gated ion channel, LGIC). Yet, elevated CO2 could induce behavioral alterations through a range of mechanisms that disturb different components of the neurobiological pathway that produces behavior, including disrupted sensation, altered behavioral choices and disturbed LGIC-mediated neurotransmission. Here, we review the potential mechanisms by which elevated CO2 may affect marine invertebrate behaviors. Marine invertebrate acid–base physiology and pharmacology is discussed in relation to altered GABAA receptor functioning. Alternative mechanisms for behavioral change at elevated CO2 are considered and important topics for future research have been identified. A mechanistic understanding will be important to determine why there is variability in elevated CO2-induced behavioral alterations across marine invertebrate taxa, why some, but not other, behaviors are affected within a species and to identify which marine invertebrates will be most vulnerable to rising CO2 levels

Quantifying pCO₂ in biological ocean acidification experiments: a comparison of four methods

Quantifying the amount of carbon dioxide (CO₂) in seawater is an essential component of ocean acidification research; however, equipment for measuring CO₂ directly can be costly and involve complex, bulky apparatus. Consequently, other parameters of the carbonate system, such as pH and total alkalinity (AT), are often measured and used to calculate the partial pressure of CO₂ (pCO₂) in seawater, especially in biological CO₂-manipulation studies, including large ecological experiments and those conducted at field sites. Here we compare four methods of pCO₂ determination that have been used in biological ocean acidification experiments: 1) Versatile INstrument for the Determination of Total inorganic carbon and titration Alkalinity (VINDTA) measurement of dissolved inorganic carbon (CT) and AT, 2) spectrophotometric measurement of pHT and AT, 3) electrode measurement of pHNBS and AT, and 4) the direct measurement of CO₂ using a portable CO₂ equilibrator with a non-dispersive infrared (NDIR) gas analyser. In this study, we found these four methods can produce very similar pCO₂ estimates, and the three methods often suited to field-based application (spectrophotometric pHT, electrode pHNBS and CO₂ equilibrator) produced estimated measurement uncertainties of 3.5–4.6% for pCO₂. Importantly, we are not advocating the replacement of established methods to measure seawater carbonate chemistry, particularly for high-accuracy quantification of carbonate parameters in seawater such as open ocean chemistry, for real-time measures of ocean change, nor for the measurement of small changes in seawater pCO₂. However, for biological CO₂-manipulation experiments measuring differences of over 100 μatm pCO₂ among treatments, we find the four methods described here can produce similar results with careful use

Ocean acidification alters predator behaviour and reduces predation rate

Ocean acidification poses a range of threats to marine invertebrates; however, the emerging and likely widespread effects of rising carbon dioxide (CO₂) levels on marine invertebrate behaviour are still little understood. Here, we show that ocean acidification alters and impairs key ecological behaviours of the predatory cone snail Conus marmoreus. Projected near-future seawater CO₂ levels (975 µatm) increased activity in this coral reef molluscivore more than threefold (from less than 4 to more than 12 mm min⁻¹) and decreased the time spent buried to less than one-third when compared with the present-day control conditions (390 µatm). Despite increasing activity, elevated CO₂ reduced predation rate during predator–prey interactions with control-treated humpbacked conch, Gibberulus gibberulus gibbosus; 60% of control predators successfully captured and consumed their prey, compared with only 10% of elevated CO₂ predators. The alteration of key ecological behaviours of predatory invertebrates by near-future ocean acidification could have potentially far-reaching implications for predator–prey interactions and trophic dynamics in marine ecosystems. Combined evidence that the behaviours of both species in this predator–prey relationship are altered by elevated CO₂ suggests food web interactions and ecosystem structure will become increasingly difficult to predict as ocean acidification advances over coming decades

Science-Based Policy Plan for Australia\u27s Coral Reefs

Australia’s coral reefs are currently under threat from a range of short-­‐ and long-­‐term stressors. The ability of corals to recover from acute disturbance events, such as bleaching, cyclones and crown-­of-thorns seastars outbreaks, is greatly influenced by the multitude of stressors reefs are currently experiencing (1). Since healthy coral habitat is essential for the persistence of associated fish and invertebrate communities, as well as the industries that rely on them (2), all possible action must be taken to reduce stress factors to corals and associated organisms. Practical changes to current reef policies will reverse the decline in the health of Australia’s coral reefs and increase the viability of all of the reef’s associated industries

Elevated temperature and carbon dioxide levels alter growth rates and shell composition in the fluted giant clam, Tridacna squamosa

Giant clams produce massive calcified shells with important biological (e.g., defensive) and ecological (e.g., habitat-forming) properties. Whereas elevated seawater temperature is known to alter giant clam shell structure, no study has examined the effects of a simultaneous increase in seawater temperature and partial pressure of carbon dioxide (pCO2) on shell mineralogical composition in these species. We investigated the effects of 60-days exposure to end-of-the-century projections for seawater temperature (+ 3 °C) and pCO2 (+ 500 µatm) on growth, mineralogy, and organic content of shells and scutes in juvenile Tridacna squamosa giant clams. Elevated temperature had no effect on growth rates or organic content, but did increase shell [24Mg]/[40Ca] as well as [40Ca] in newly-formed scutes. Elevated pCO2 increased shell growth and whole animal mass gain. In addition, we report the first evidence of an effect of elevated pCO2 on element/Ca ratios in giant clam shells, with significantly increased [137Ba]/[40Ca] in newly-formed shells. Simultaneous exposure to both drivers greatly increased inter-individual variation in mineral concentrations and resulted in reduced shell N-content which may signal the onset of physiological stress. Overall, our results indicate a greater influence of pCO2 on shell mineralogy in giant clams than previously recognized

The role of ligand-gated chloride channels in behavioural alterations at elevated CO2 in a cephalopod

Projected future carbon dioxide (CO2) levels in the ocean can alter marine animal behaviours. Disrupted functioning of γ-aminobutyric acid type A (GABAA) receptors (ligand-gated chloride channels) is suggested to underlie CO2-induced behavioural changes in fish. However, the mechanisms underlying behavioural changes in marine invertebrates are poorly understood. We pharmacologically tested the role of GABA-, glutamate-, acetylcholine- and dopamine-gated chloride channels in CO2-induced behavioural changes in a cephalopod, the two-toned pygmy squid (Idiosepius pygmaeus). We exposed squid to ambient (~450 μatm) or elevated (~1000 μatm) CO2 for 7 days. Squid were treated with sham, the GABAA receptor antagonist gabazine or the non-specific GABAA receptor antagonist picrotoxin, before measurement of conspecific-directed behaviours and activity levels upon mirror exposure. Elevated CO2 increased conspecific-directed attraction and aggression, as well as activity levels. For some CO2-affected behaviours, both gabazine and picrotoxin had a different effect at elevated compared with ambient CO2, providing robust support for the GABA hypothesis within cephalopods. In another behavioural trait, picrotoxin but not gabazine had a different effect in elevated compared with ambient CO2, providing the first pharmacological evidence, in fish and marine invertebrates, for altered functioning of ligand-gated chloride channels, other than the GABAAR, underlying CO2-induced behavioural changes. For some other behaviours, both gabazine and picrotoxin had a similar effect in elevated and ambient CO2, suggesting altered function of ligand-gated chloride channels was not responsible for these CO2-induced changes. Multiple mechanisms may be involved, which could explain the variability in the CO2 and drug treatment effects across behaviours

The Effects of Salinity and pH on Fertilization, Early Development and Hatching in the Crown-of-Thorns Seastar

Understanding the influence of environmental factors on the development and dispersal of crown-of-thorns seastars is critical to predicting when and where outbreaks of these coral-eating seastars will occur. Outbreaks of the crown-of-thorns seastars are hypothesized to be driven by terrestrial runoff events that increase nutrients and the phytoplankton food for the larvae. In addition to increasing larval food supply, terrestrial runoff may also reduce salinity in the waters where seastars develop. We investigated the effects of reduced salinity on the fertilisation and early development of seastars, up to and including their hatching from the fertilisation envelope. We also tested the interactive effects of reduced salinity and reduced pH on the hatching of crown-of-thorns seastars. Overall, we found that reduced salinity has strong negative effects on fertilisation and early development, as has been shown in other echinoderm species. We also found that reduced salinity delays hatching but that reduced pH, in isolation or in combination with lower salinity, had no detectable effects on this developmental milestone. Models that assess the positive effects of terrestrial runoff on the development of crown-of-thorns seastars should also consider the strong negative effects of lower salinity on early development including lower levels of fertilisation, increased frequency of abnormal development and delayed time to hatching