Have we been underestimating the effects of ocean acidification in zooplankton?

Understanding how copepods may respond to ocean acidification (OA) is critical for risk assessments of ocean ecology and biogeochemistry. The perception that copepods are insensitive to OA is largely based on experiments with adult females. Their apparent resilience to increased carbon dioxide (pCO2 ) concentrations has supported the view that copepods are 'winners' under OA. Here, we show that this conclusion is not robust, that sensitivity across different life stages is significantly misrepresented by studies solely using adult females. Stage-specific responses to pCO2 (385-6000 μatm) were studied across different life stages of a calanoid copepod, monitoring for lethal and sublethal responses. Mortality rates varied significantly across the different life stages, with nauplii showing the highest lethal effects; nauplii mortality rates increased threefold when pCO2 concentrations reached 1000 μatm (year 2100 scenario) with LC50 at 1084 μatm pCO2 . In comparison, eggs, early copepodite stages, and adult males and females were not affected lethally until pCO2 concentrations ≥3000 μatm. Adverse effects on reproduction were found, with >35% decline in nauplii recruitment at 1000 μatm pCO2 . This suppression of reproductive scope, coupled with the decreased survival of early stage progeny at this pCO2 concentration, has clear potential to damage population growth dynamics in this species. The disparity in responses seen across the different developmental stages emphasizes the need for a holistic life-cycle approach to make species-level projections to climate change. Significant misrepresentation and error propagation can develop from studies which attempt to project outcomes to future OA conditions solely based on single life history stage exposures.

Microsporidia-nematode associations in methane seeps reveal basal fungal parasitism in the deep sea

The deep sea is Earth’s largest habitat but little is known about the nature of deep-sea parasitism. In contrast to a few characterized cases of bacterial and protistan parasites, the existence and biological significance of deep-sea parasitic fungi is yet to be understood. Here we report the discovery of a fungus-related parasitic microsporidium, Nematocenator marisprofundi n. gen. n. sp. that infects benthic nematodes at Pacific Ocean methane seeps on the Pacific Ocean floor. This infection is species-specific and has been temporally and spatially stable over two years of sampling, indicating an ecologically consistent host-parasite interaction. A high distribution of spores in the reproductive tracts of infected males and females and their absence from host nematodes’ intestines suggests a sexual transmission strategy in contrast to the fecal-oral transmission of most microsporidia. N. marisprofundi targets the host’s body wall muscles causing cell lysis, and in severe infection even muscle filament degradation. Phylogenetic analyses placed N. marisprofundi in a novel and basal clade not closely related to any described microsporidia clade, suggesting either that microsporidia-nematode parasitism occurred early in microsporidia evolution or that host specialization occurred late in an ancient deep-sea microsporidian lineage. Our findings reveal that methane seeps support complex ecosystems involving interkingdom interactions between bacteria, nematodes, and parasitic fungi and that microsporidia parasitism exists also in the deep sea biosphere.

Feeding and overwintering of Antarctic krill across its major habitats: The role of sea ice cover, water depth, and phytoplankton abundance

Antarctic krill (Euphausia superba) were sampled in contrasting habitats: a seasonally ice-covered deep ocean (Lazarev Sea), ice-free shelves at their northern range (South Georgia) and the Antarctic Peninsula (Bransfield Strait), and shelf and oceanic sites in the Scotia Sea. Across 92 stations, representing a year-round average, the food volume in krill stomachs comprised 71 +/- 29% algae, 17 +/- 21% protozoans, and 12 +/- 25% metazoans. Fatty acid trophic markers showed that copepods were consistently part of krill diet, not a switch food. In open waters, both diatom and copepod consumption increased with phytoplankton abundance. Under sea ice, ingestion of diatoms became rare, whereas feeding on copepods remained constant. During winter, larvae contained high but variable proportions of diatom markers, whereas in postlarvae the role of copepods increased with krill body length. Overwintering differed according to habitat. Krill from South Georgia had lower lipid stores than those from the Bransfield Strait or Lazarev Sea. Feeding effort was much reduced in Lazarev Sea krill, whereas most individuals from the Bransfield Strait and South Georgia contained phytoplankton and seabed detritus in their stomachs. Their retention of essential body reserves indicates that krill experienced most winter hardship in the Lazarev Sea, followed by South Georgia and then Bransfield Strait. This was reflected in the delayed development from juveniles to adults in the Lazarev Sea. Circumpolar comparisons of length frequencies suggest that krill growth conditions are more favorable in the southwest Atlantic than in the Lazarev Sea or off East Antarctica because of longer phytoplankton bloom periods and rewarding access to benthic food.

Oithona similislikes it cool: evidence from two long-term time series

We compare the long-term and seasonal patterns of abundance and phenology of the cyclopoid copepod Oithona similis at the L4 site (1988–2013) in the North Atlantic and at the LTER-MC site (1984–2013) in the Mediterranean Sea to investigate whether high temperature limits the occurrence of this species with latitudinal cline. The two sites are well suited to testing this hypothesis as they are characterized by similar chlorophyll a concentration (Chl a) but different temperature [sea surface temperature (SST)]. The abundance of O. similis at L4 was ∼10 times higher than at LTER-MC. Moreover, this species had several peaks of abundance during the year at L4 but a single peak in spring at LTER-MC. The main mode of temporal variability in abundance was seasonal at both sites. The abundance of O. similis was negatively correlated with SST only at LTER-MC, whereas it was positively correlated with Chl a at both sites. Oithona similis had a temperature optimum between 15 and 20°C reaching maximum abundance at ∼16.5°C at LTER-MC, but showed no Chl a optimum at either site. We conclude that the abundance of O. similis increases with prey availability up to 16.5°C and that temperature >20°C represents the main limiting factor for population persistence.

The Impact of Polystyrene Microplastics on Feeding, Function and Fecundity in the Marine CopepodCalanus helgolandicus

Microscopic plastic debris, termed “microplastics”, are of increasing environmental concern. Recent studies have demonstrated that a range of zooplankton, including copepods, can ingest microplastics. Copepods are a globally abundant class of zooplankton that form a key trophic link between primary producers and higher trophic marine organisms. Here we demonstrate that ingestion of microplastics can significantly alter the feeding capacity of the pelagic copepod Calanus helgolandicus. Exposed to 20 μm polystyrene beads (75 microplastics mL–1) and cultured algae ([250 μg C L–1) for 24 h, C. helgolandicus ingested 11% fewer algal cells (P = 0.33) and 40% less carbon biomass (P < 0.01). There was a net downward shift in the mean size of algal prey consumed (P < 0.001), with a 3.6 fold increase in ingestion rate for the smallest size class of algal prey (11.6–12.6 μm), suggestive of postcapture or postingestion rejection. Prolonged exposure to polystyrene microplastics significantly decreased reproductive output, but there were no significant differences in egg production rates, respiration or survival. We constructed a conceptual energetic (carbon) budget showing that microplastic-exposed copepods suffer energetic depletion over time. We conclude that microplastics impede feeding in copepods, which over time could lead to sustained reductions in ingested carbon biomass.

Next Generation Sequencing Reveals the Hidden Diversity of Zooplankton Assemblages

Zooplankton play an important role in our oceans, in biogeochemical cycling and providing a food source for commercially important fish larvae. However, difficulties in correctly identifying zooplankton hinder our understanding of their roles in marine ecosystem functioning, and can prevent detection of long term changes in their community structure. The advent of massively parallel next generation sequencing technology allows DNA sequence data to be recovered directly from whole community samples. Here we assess the ability of such sequencing to quantify richness and diversity of a mixed zooplankton assemblage from a productive time series site in the Western English Channel. Methodology/Principle Findings Plankton net hauls (200 µm) were taken at the Western Channel Observatory station L4 in September 2010 and January 2011. These samples were analysed by microscopy and metagenetic analysis of the 18S nuclear small subunit ribosomal RNA gene using the 454 pyrosequencing platform. Following quality control a total of 419,041 sequences were obtained for all samples. The sequences clustered into 205 operational taxonomic units using a 97% similarity cut-off. Allocation of taxonomy by comparison with the National Centre for Biotechnology Information database identified 135 OTUs to species level, 11 to genus level and 1 to order, <2.5% of sequences were classified as unknowns. By comparison a skilled microscopic analyst was able to routinely enumerate only 58 taxonomic groups. Conclusions Metagenetics reveals a previously hidden taxonomic richness, especially for Copepoda and hard-to-identify meroplankton such as Bivalvia, Gastropoda and Polychaeta. It also reveals rare species and parasites. We conclude that Next Generation Sequencing of 18S amplicons is a powerful tool for elucidating the true diversity and species richness of zooplankton communities. While this approach allows for broad diversity assessments of plankton it may become increasingly attractive in future if sequence reference libraries of accurately identified individuals are better populated.

Contrasting transcriptome response to thermal stress in two key zooplankton species, Calanus finmarchicus and C. glacialis

Climate change has already led to the range expansion of warm-water plankton assemblages in the northeast Atlantic and the corresponding range contraction of colder-water species. The temperate copepod Calanus finmarchicus is predicted to shift farther northward into polar waters traditionally dominated by the arctic copepod C. glacialis. To identify temperaturemediated changes in gene expression that may be critical for the thermal acclimation and resilience of the 2 Calanus spp., we conducted a whole transcriptome profiling using RNA-seq on an Ion Torrent platform. Transcriptome responses of C. finmarchicus and C. glacialis from Disko Bay, west Greenland, were investigated under realistic thermal stresses (at + 5, +10 and +15°C) for 4 h and 6 d. C. finmarchicus showed a strong response to temperature and duration of stress, involving up-regulation of genes related to protein folding, transcription, translation and metabolism. In sharp contrast, C. glacialis displayed only low-magnitude changes in gene expression in response to temperature and duration of stress. Differences in the thermal responses of the 2 species, particularly the lack of thermal stress response in C. glacialis, are in line with laboratory and field observations and suggest a vulnerability of C. glacialis to climate change.

How does Calanus helgolandicus maintain its population in a variable environment? Analysis of a 25-year time series from the English Channel

Calanus helgolandicus is a key copepod of the NE Atlantic and fringing shelves, with a distribution that is expanding northwards with oceanic warming. The Plymouth L4 site has warmed over the past 25-years, and experiences large variations in the timing and availability of food for C. helgolandicus. Here we examine the degree to which these changes translate into variation in reproductive output and subsequently C. helgolandicus population size. Egg production rates (eggs female−1 day−1) were maximal in the spring to early-summer period of diatom blooms and high ciliate abundance, rather than during the equally large autumn blooms of autotrophic dinoflagellates. Egg hatch success was lower in spring however, with a greater proportion of naupliar deformities then also. Both the timing and the mean summer abundance of C. helgolandicus (CI–CVI) reflected those of spring total reproductive output. However this relationship was driven by inter-annual variability in female abundance and not that of egg production per female, which ranged only two-fold. Winter abundance of C. helgolandicus at L4 was much more variable than abundance in other seasons, and reflected conditions from the previous growing season. However, these low winter abundances had no clear carry-over signal to the following season’s population size. Overall, the C. helgolandicus population appears to be surprisingly resilient at this dynamic, inshore site, showing no long-term phenology shift and only a four-fold variation in mean abundance between years. This dampening effect may reflect a series of mortality sources, associated with the timing of stratification in the early part of the season, likely affecting egg sinking and loss, plus intense, density-dependent mortality of early stages in mid-summer likely through predation.

Female-biased sex ratios in marine pelagic copepods: comment on Gusmao et al

Gusmão et al. (2013; Mar Ecol Prog Ser 482:279-298) review causes of sex ratio skew in pelagic copepods and in doing so repeatedly dispute the paper of Hirst et al. (2010) ‘Does predation control adult sex ratios and longevities in marine pelagic copepods?’ Here we respond to some important errors in their citation of our paper and briefly highlight where future work is needed in order to attribute the causes of strong sex ratio skew seen in some copepod families.

Microplastics Alter the Properties and Sinking Rates of Zooplankton Faecal Pellets

Plastic debris is a widespread contaminant, prevalent in aquatic ecosystems across the globe. Zooplankton readily ingest microscopic plastic (microplastic, < 1 mm), which are later egested within their faecal pellets. These pellets are a source of food for marine organisms, and contribute to the oceanic vertical flux of particulate organic matter as part of the biological pump. The effects of microplastics on faecal pellet properties are currently unknown. Here we test the hypotheses that (1) faecal pellets are a vector for transport of microplastics, (2) polystyrene microplastics can alter the properties and sinking rates of zooplankton egests and, (3) faecal pellets can facilitate the transfer of plastics to coprophagous biota. Following exposure to 20.6 μm polystyrene microplastics (1000 microplastics mL–1) and natural prey (∼1650 algae mL–1) the copepod Calanus helgolandicus egested faecal pellets with significantly (P < 0.001) reduced densities, a 2.25-fold reduction in sinking rates, and a higher propensity for fragmentation. We further show that microplastics, encapsulated within egests of the copepod Centropages typicus, could be transferred to C. helgolandicus via coprophagy. Our results support the proposal that sinking faecal matter represents a mechanism by which floating plastics can be vertically transported away from surface waters.

Modelling the future biogeography of North Atlantic zooplankton communities in response to climate change

Advances in habitat and climate modelling allow us to reduce uncertainties of climate change impacts on species distribution. We evaluated the impacts of future climate change on community structure, diversity, distribution and phenology of 14 copepod species in the North Atlantic. We developed and validated habitat models for key zooplankton species using continuous plankton recorder (CPR) survey data collected at mid latitudes of the North Atlantic. Generalized additive models (GAMs) were applied to relate the occurrence of species to environmental variables. Models were projected to future (2080–2099) environmental conditions using coupled hydroclimatix–biogeochemical models under the Intergovernmental Panel on Climate Change (IPCC) A1B climate scenario, and compared to present (2001–2020) conditions. Our projections indicated that the copepod community is expected to respond substantially to climate change: a mean poleward latitudinal shift of 8.7 km per decade for the overall community with an important species range variation (–15 to 18 km per decade); the species seasonal peak is expected to occur 12–13 d earlier for Calanus finmarchicus and C. hyperboreus; and important changes in community structure are also expected (high species turnover of 43–79% south of the Oceanic Polar Front). The impacts of the change expected by the end of the century under IPCC global warming scenarios on copepods highlight poleward shifts, earlier seasonal peak and changes in biodiversity spatial patterns that might lead to alterations of the future North Atlantic pelagic ecosystem. Our model and projections are supported by a temporal validation undertaken using the North Atlantic climate regime shift that occurred in the 1980s: the habitat model built in the cold period (1970–1986) has been validated in the warm period (1987–2004).