Impaired learning of predators and lower prey survival under elevated CO2: a consequence of neurotransmitter interference

Ocean acidification is one of the most pressing environmental concerns of our time, and not surprisingly, we have seen a recent explosion of research into the physiological impacts and ecological consequences of changes in ocean chemistry. We are gaining considerable insights from this work, but further advances require greater integration across disciplines. Here, we showed that projected near-future CO2 levels impaired the ability of damselfish to learn the identity of predators. These effects stem from impaired neurotransmitter function; impaired learning under elevated CO2 was reversed when fish were treated with gabazine, an antagonist of the GABA-A receptor - a major inhibitory neurotransmitter receptor in the brain of vertebrates. The effects of CO2 on learning and the link to neurotransmitter interference were manifested as major differences in survival for fish released into the wild. Lower survival under elevated CO2 , as a result of impaired learning, could have a major influence on population recruitment.

Seawater carbonate chemistry, fertilization and early development of the coral eating crown-of-thorns starfish, Acanthaster planci in a laboratory experiment

Outbreaks of crown-of-thorns starfish (COTS), Acanthaster planci, contribute to major declines of coral reef ecosystems throughout the Indo-Pacific. As the oceans warm and decrease in pH due to increased anthropogenic CO2 production, coral reefs are also susceptible to bleaching, disease and reduced calcification. The impacts of ocean acidification and warming may be exacerbated by COTS predation, but it is not known how this major predator will fare in a changing ocean. Because larval success is a key driver of population outbreaks, we investigated the sensitivities of larval A. planci to increased temperature (2-4 °C above ambient) and acidification (0.3-0.5 pH units below ambient) in flow-through cross-factorial experiments (3 temperature × 3 pH/pCO2 levels). There was no effect of increased temperature or acidification on fertilization or very early development. Larvae reared in the optimal temperature (28 °C) were the largest across all pH treatments. Development to advanced larva was negatively affected by the high temperature treatment (30 °C) and by both experimental pH levels (pH 7.6, 7.8). Thus, planktonic life stages of A. planci may be negatively impacted by near-future global change. Increased temperature and reduced pH had an additive negative effect on reducing larval size. The 30 °C treatment exceeded larval tolerance regardless of pH. As 30 °C sea surface temperatures may become the norm in low latitude tropical regions, poleward migration of A. planci may be expected as they follow optimal isotherms. In the absence of acclimation or adaptation, declines in low latitude populations may occur. Poleward migration will be facilitated by strong western boundary currents, with possible negative flow-on effects on high latitude coral reefs. The contrasting responses of the larvae of A. planci and those of its coral prey to ocean acidification and warming are considered in context with potential future change in tropical reef ecosystems.

Conflicting effects of predator cue and ocean acidification on the mussel Mytilus coruscus byssus production

Understanding the impact of ocean acidification and warming on communities and ecosystems is a researcher priority. This can only be achieved through a combination of experimental and field approaches that would allow developing a mechanistic understanding of impacts across level of biological organizations. Surprisingly, most published studies are still focusing on single species responses with little consideration for interspecific interactions. In this study, the impacts of a 3 days exposure to three parameters (temperature, pH, and presence/absence of the predator cue of the crab Charybdis japonica) and their interactions on an ecologically important endpoint were evaluated: the byssus production of the mussel Mytilus coruscus. Tested temperatures (25°C and 30°C) were within the present range of natural variability whereas pH (8.1, 7.7, and 7.4) covered present as well as near-future natural variability. As expected, the presence of the crab cue induced an antipredator response in Mytilus coruscus (significant 10% increase in byssus secretion rate, 22% increase in frequency of shed byssus, and 30% longer byssus). Decreased pH but not temperature had a significant negative impact on the same endpoints (up to a 17% decrease in byssus secretion rate, 40% decrease in frequency of shed byssus, and 10% shorter byssus at pH 7.3 as compared with pH 8.1) with no significant interactions between the three tested parameters. In this study, it has been hypothesized that pH and predator cue have different modes of action and lead to conflicting functional responses (escape response versus stronger attachment). Functional consequences for ecosystem dynamics still need to be investigated.

Populations of Pacific Oysters Crassostrea gigas Respond Variably to Elevated CO2 and Predation by Morula marginalba

Ocean acidification is anticipated to decrease calcification and increase dissolution of shelled molluscs. Molluscs with thinner and weaker shells may be more susceptible to predation, but not all studies have measured negative responses of molluscs to elevated pCO2. Recent studies measuring the response of molluscs have found greater variability at the population level than first expected. Here we investigate the impact of acidification on the predatory whelk Morula marginalba and genetically distinct subpopulations of the Pacific oyster Crassostrea gigas. Whelks and eight family lines of C. gigas were separately exposed to ambient (385 ppm) and elevated (1000 ppm) pCO2 for 6 weeks. Following this period, individuals of M. marginalba were transferred into tanks with oysters at ambient and elevated pCO2 for 17 days. The increase in shell height of the oysters was on average 63% less at elevated compared to ambient pCO2. There were differences in shell compression strength, thickness, and mass among family lines of C. gigas, with sometimes an interaction between pCO2 and family line. Against expectations, this study found increased shell strength in the prey and reduced shell strength in the predator at elevated compared to ambient pCO2. After 10 days, the whelks consumed significantly more oysters regardless of whether C. gigas had been exposed to ambient or elevated CO2, but this was not dependent on the family line and the effect was not significant after 17 days. Our study found an increase in predation after exposure of the predator to predicted near-future levels of estuarine pCO2.

Effects of ocean acidification on learning in coral reef fishes

Ocean acidification has the potential to cause dramatic changes in marine ecosystems. Larval damselfish exposed to concentrations of CO2 predicted to occur in the mid- to late-century show maladaptive responses to predator cues. However, there is considerable variation both within and between species in CO2 effects, whereby some individuals are unaffected at particular CO2 concentrations while others show maladaptive responses to predator odour. Our goal was to test whether learning via chemical or visual information would be impaired by ocean acidification and ultimately, whether learning can mitigate the effects of ocean acidification by restoring the appropriate responses of prey to predators. Using two highly efficient and widespread mechanisms for predator learning, we compared the behaviour of pre-settlement damselfish Pomacentrus amboinensis that were exposed to 440 µatm CO2 (current day levels) or 850 µatm CO2, a concentration predicted to occur in the ocean before the end of this century. We found that, regardless of the method of learning, damselfish exposed to elevated CO2 failed to learn to respond appropriately to a common predator, the dottyback, Pseudochromis fuscus. To determine whether the lack of response was due to a failure in learning or rather a short-term shift in trade-offs preventing the fish from displaying overt antipredator responses, we conditioned 440 or 700 µatm-CO2 fish to learn to recognize a dottyback as a predator using injured conspecific cues, as in Experiment 1. When tested one day post-conditioning, CO2 exposed fish failed to respond to predator odour. When tested 5 days post-conditioning, CO2 exposed fish still failed to show an antipredator response to the dottyback odour, despite the fact that both control and CO2-treated fish responded to a general risk cue (injured conspecific cues). These results indicate that exposure to CO2 may alter the cognitive ability of juvenile fish and render learning ineffective.

Stomach content records for pelagic fish (herring, mackerel, blue whiting, albacore and bluefin tuna) in the northeast Atlantic

Fish stomach content records extracted from the DAPSTOM 4.5 database (held at the UK Centre for Environment, Fisheries and Aquaculture Science - CEFAS). Data collated as part of the EU Euro-Basin project and specifically concerning herring (Clupea harengus), mackerel (Scomber scombrus), blue whiting (Micromesistius poutassou), albacore (Thunnus alalunga) and bluefin tuna (Thunnus thynnus). The data set consist of 20720 records - collected throughout the northeast Atlantic, between 1906 and 2011 - mostly during routine fisheries monitoring research cruises.

Direct linkage between dimethyl sulfide production and microzooplankton grazing, resulting from prey composition change under high partial pressure of carbon dioxide conditions

Oceanic dimethyl sulfide (DMS) is the enzymatic cleavage product of the algal metabolite dimethylsulfoniopropionate (DMSP) and is the most abundant form of sulfur released into the atmosphere. To investigate the effects of two emerging environmental threats (ocean acidification and warming) on marine DMS production, we performed a large-scale perturbation experiment in a coastal environment. At both ambient temperature and 2 °C warmer, an increase in partial pressure of carbon dioxide (pCO2) in seawater (160-830 ppmv pCO2) favored the growth of large diatoms, which outcompeted other phytoplankton species in a natural phytoplankton assemblage and reduced the growth rate of smaller, DMSP-rich phototrophic dinoflagellates. This decreased the grazing rate of heterotrophic dinoflagellates (ubiquitous micrograzers), resulting in reduced DMS production via grazing activity. Both the magnitude and sign of the effect of pCO2 on possible future oceanic DMS production were strongly linked to pCO2-induced alterations to the phytoplankton community and the cellular DMSP content of the dominant species and its association with micrograzers.

Life-history traits of two Salvelinus species and mercury concentrations in fish and prey in ten Canadian lakes (2006-2008)

Mercury concentrations ([Hg]) in Arctic food fish often exceed guidelines for human subsistence consumption. Previous research on two food fish species, Arctic char (Salvelinus alpinus) and lake trout (Salvelinus namaycush), indicates that anadromous fish have lower [Hg] than nonanadromous fish, but there have been no intraregional comparisons. Also, no comparisons of [Hg] among anadromous (sea-run), resident (marine access but do not migrate), and landlocked (no marine access) life history types of Arctic char and lake trout have been published. Using intraregional data from 10 lakes in the West Kitikmeot area of Nunavut, Canada, we found that [Hg] varied significantly among species and life history types. Differences among species-life history types were best explained by age-at-size and C:N ratios (indicator of lipid); [Hg] was significantly and negatively related to both. At a standardized fork length of 500 mm, lake trout had significantly higher [Hg] (mean 0.17 µg/g wet wt) than Arctic char (0.09 µg/g). Anadromous and resident Arctic char had significantly lower [Hg] (each 0.04 µg/g) than landlocked Arctic char (0.19 µg/g). Anadromous lake trout had significantly lower [Hg] (0.12 µg/g) than resident lake trout (0.18 µg/g), but no significant difference in [Hg] was seen between landlocked lake trout (0.21 µg/g) and other life history types. Our results are relevant to human health assessments and consumption guidance and will inform models of Hg accumulation in Arctic fish.

Fatty acid composition of tissue samples from Arctic walruses (Odobenus rosmarus rosmarus) and their prey

Blubber biopsies were collected from 18 adult male walruses from Svalbard, Norway. The biopsies were taken vertically through the skin and the entire blubber layer down to, but not including, the muscle layer. Fatty acid (FA) compositions of inner blubber, outer blubber and dermis of the walruses and of potential prey organisms were determined. The three layers differed significantly from one another in FA composition. Generally, the inner blubber contained more long-chained monounsaturated, saturated and polyunsaturated FAs, while the outer blubber and dermis contained more short-chained monounsaturated FAs. This stratification is similar to what has been observed in other marine mammal species. However, differences between layers were less pronounced than in most other species, possibly because the extremely thick overlying dermis of walruses provides an insulating shield, which affects the FA composition of the outer blubber. The FA composition of the potential prey organisms was different from that of the blubber of the walruses, although more similar to the inner blubber than to the outer blubber or dermis. FA composition in the inner blubber was not significantly correlated with age (assessed by tusk volume), while the FA composition of the outer blubber and dermis were significantly correlated with age.

Bird predation experiments in tropical agroforestry landscapes of the Napu Valley in Central Sulawesi, Indonesia

We performed bird predation experiments (dummy experiments), using artificial prey and bird community data to investigate the importance of predator diversity vs. predator identity in cacao agroforestry landscapes. All sample sites were situated at the northern tip of Napu Valley in Central Sulawesi, Indonesia. After an initial mapping of the study area, we selected 15 smallholder cacao plantations as sites for our exclosure experiments in March 2010. For our predation experiment, we selected 10 (out of 15) study sites and 5 cacao trees per site for the application of artificial prey for birds (dummy caterpillars made of plasticine). Our study trees (numbered from 1 to 5 per site) were randomly chosen and we kept spacing of at least two unmanipulated cacao trees between two study trees to avoid clumped distribution. To quantify both daytime/diurnal predation and night-time/nocturnal predation (e.g. birds vs. bats), we applied 7 caterpillar dummies on all study trees and controlled them for predation marks in the early morning (05:00-06:00 am), in the evening (17:00-18:00 pm) and in the early morning on the next day (completing one survey round). In total, we performed four survey rounds per study site (in June and July 2011). The caterpillar dummies were always applied in the same order and on three different parts of each cacao study tree: One 'control dummy' (located on first branching of the cacao tree); 3 'branch dummies' (located on one main branch coming from first branching; 20-25 cm between single dummies) and 3 'leaf dummies' (3 medium aged cacao trees adjacent to main branch were selected and single dummies placed in the center of each cacao leaf). The different positions were chosen to control for different foraging modes of predators (e.g. branch gleaners versus leaf gleaners). During day- and nighttime surveys, we controlled if the dummy caterpillars were still present in their original position, if they were absent and could not be relocated on the ground or if they were fallen to the ground, but could still be recorded. Eaten dummies were counted as 1 mark usually, except for those dummies, where two or more different kind of arthropods had eaten parts of the dummy (2 marks or more). Other predation marks were added to this number. For each dummy, we counted the total number of different predation marks. We focused on predation marks that could be identified with certainty (based on preliminary observations and/or literature): marks of birds, rodents and snails. Finally, we analysed the relationship of bird predation marks and bird community parameters (abundance vs. diversity), as well as effects of local and landscape management on the avian predation success.