The impacts of past, present and future ocean chemistry on predatory planktonic snails.

The atlantid heteropods represent the only predatory, aragonite shelled zooplankton. Atlantid shell production is likely to be sensitive to ocean acidification (OA), and yet we know little about their mechanisms of calcification, or their response to changing ocean chemistry. Here, we present the first study into calcification and gene expression effects of short-term OA exposure on juvenile atlantids across three pH scenarios: mid-1960s, ambient and 2050 conditions. Calcification and gene expression indicate a distinct response to each treatment. Shell extension and shell volume were reduced from the mid-1960s to ambient conditions, suggesting that calcification is already limited in today's South Atlantic. However, shell extension increased from ambient to 2050 conditions. Genes involved in protein synthesis were consistently upregulated, whereas genes involved in organismal development were downregulated with decreasing pH. Biomineralization genes were upregulated in the mid-1960s and 2050 conditions, suggesting that any deviation from ambient carbonate chemistry causes stress, resulting in rapid shell growth. We conclude that atlantid calcification is likely to be negatively affected by future OA. However, we also found that plentiful food increased shell extension and shell thickness, and so synergistic factors are likely to impact the resilience of atlantids in an acidifying ocean.

Pteropods make thinner shells in the upwelling region of the California Current Ecosystem.

Shelled pteropods are widely regarded as bioindicators for ocean acidification, because their fragile aragonite shells are susceptible to increasing ocean acidity. While short-term incubations have demonstrated that pteropod calcification is negatively impacted by ocean acidification, we know little about net calcification in response to varying ocean conditions in natural populations. Here, we examine in situ calcification of Limacina helicina pteropods collected from the California Current Ecosystem, a coastal upwelling system with strong spatial gradients in ocean carbonate chemistry, dissolved oxygen and temperature. Depth-averaged pH ranged from 8.03 in warmer offshore waters to 7.77 in cold CO2-rich waters nearshore. Based on high-resolution micro-CT technology, we showed that shell thickness declined by ~ 37% along the upwelling gradient from offshore to nearshore water. Dissolution marks covered only ~ 2% of the shell surface area and were not associated with the observed variation in shell thickness. We thus infer that pteropods make thinner shells where upwelling brings more acidified and colder waters to the surface. Probably the thinner shells do not result from enhanced dissolution, but are due to a decline in calcification. Reduced calcification of pteropods is likely to have major ecological and biogeochemical implications for the cycling of calcium carbonate in the oceans.

Fossil-calibrated molecular phylogeny of atlantid heteropods (Gastropoda, Pterotracheoidea).

BACKGROUND: The aragonite shelled, planktonic gastropod family Atlantidae (shelled heteropods) is likely to be one of the first groups to be impacted by imminent ocean changes, including ocean warming and ocean acidification. With a fossil record spanning at least 100 Ma, atlantids have experienced and survived global-scale ocean changes and extinction events in the past. However, the diversification patterns and tempo of evolution in this family are largely unknown. RESULTS: Based on a concatenated maximum likelihood phylogeny of three genes (cytochrome c oxidase subunit 1 mitochondrial DNA, 28S and 18S ribosomal rRNA) we show that the three extant genera of the family Atlantidae, Atlanta, Protatlanta and Oxygyrus, form monophyletic groups. The genus Atlanta is split into two groups, one exhibiting smaller, well ornamented shells, and the other having larger, less ornamented shells. The fossil record, in combination with a fossil-calibrated phylogeny, suggests that large scale atlantid extinction was accompanied by considerable and rapid diversification over the last 25 Ma, potentially driven by vicariance events. CONCLUSIONS: Now confronted with a rapidly changing modern ocean, the ability of atlantids to survive past global change crises gives some optimism that they may be able to persist through the Anthropocene.

Stable coexistence of equivalent nutrient competitors through niche differentiation in the light spectrum.

Niche-based theories and the neutral theory of biodiversity differ in their predictions of how the species composition of natural communities will respond to changes in nutrient availability. This is an issue of major environmental relevance, as many ecosystems have experienced changes in nitrogen (N) and phosphorus (P) due to anthropogenic manipulation of nutrient loading. To understand how changes in N and P limitation may impact community structure, we conducted laboratory competition experiments using a multispecies phytoplankton community sampled from the North Sea. Results showed that picocyanobacteria (Cyanobium sp.) won the competition under N limitation, while picocyanobacteria and nonmotile nanophytoplankton (Nannochloropsis sp.) coexisted at equal abundances under P limitation. Additional experiments using isolated monocultures confirmed that Cyanobium sp. depleted N to lower levels than Nannochloropsis sp., but that both species had nearly identical P requirements, suggesting a potential for neutral coexistence under P-limited conditions. Pairwise competition experiments with the two isolates seemed to support the consistency of these results, but P limitation resulted in stable species coexistence irrespective of the initial conditions rather than the random drift of species abundances predicted by neutral theory. Comparison of the light absorption spectra indicates that coexistence of the two species was stabilized through differential use of the underwater light spectrum. Our results provide an interesting experimental example of modern coexistence theory, where species were equal competitors in one niche dimension but their competitive traits differed in other niche dimensions, thus enabling stable species coexistence on a single limiting nutrient through niche differentiation in the light spectrum.

Biogeography and genetic diversity of the atlantid heteropods.

The atlantid heteropods are regularly encountered, but rarely studied marine planktonic gastropods. Relying on a small (<14 mm), delicate aragonite shell and living in the upper ocean means that, in common with pteropods, atlantids are likely to be affected by imminent ocean changes. Variable shell morphology and widespread distributions indicate that the family is more diverse than the 23 currently known species. Uncovering this diversity is fundamental to determining the distribution of atlantids and to understanding their environmental tolerances. Here we present phylogenetic analyses of all described species of the family Atlantidae using 437 new and 52 previously published cytochrome c oxidase subunit 1 mitochondrial DNA (mtCO1) sequences. Specimens and published sequences were gathered from 32 Atlantic Ocean stations, 14 Indian Ocean stations and 21 Pacific Ocean stations between 35°N and 43°S. DNA barcoding and Automatic Barcode Gap Discovery (ABGD) proved to be valuable tools for the identification of described atlantid species, and also revealed ten additional distinct clades, suggesting that the diversity within this family has been underestimated. Only two of these clades displayed obvious morphological characteristics, demonstrating that much of the newly discovered diversity is hidden from morphology-based identification techniques. Investigation of six large atlantid collections demonstrated that 61% of previously described (morpho) species have a circumglobal distribution. Of the remaining 39%, two species were restricted to the Atlantic Ocean, five occurred in the Indian and Pacific oceans, one species was only found in the northeast Pacific Ocean, and one occurred only in the Southern Subtropical Convergence Zone. Molecular analysis showed that seven of the species with wide distributions were comprised of two or more clades that occupied distinct oceanographic regions. These distributions may suggest narrower environmental tolerances than the described morphospecies. Results provide an updated biogeography and mtCO1 reference dataset of the Atlantidae that may be used to identify atlantid species and provide a first step in understanding their evolutionary history and accurate distribution, encouraging the inclusion of this family in future plankton research.