Reply to Haddock, S. H. D. Reconsidering evidence for potential climate-related increases in jellyfish

Following the publication of our paper (Attrill et al. 2007), we became quickly aware of a couple of errors. We have subsequently been collaborating with Dr. Chris Lynam (Lynam et al. 2004, 2005) to bring together our two datasets, explore the common patterns within our data, and attempt to provide a consensus on how climate is affecting gelatinous plankton in the North Sea. During this reanalysis, two errors within the data were discovered, one involving a transcription error of a column of residuals during de-trended analysis, the other a major data entry error deep in the Continuous Plankton Recorder (CPR) database for sector B2. Here we present a revised version of table 1 from Attrill et al. (2007) to incorporate corrections to these transcription and data entry errors. These corrections alter some of the results in our original data table, mainly to increase and strengthen the number of significant relations we found (e.g., for sector B2 and whole sea area); all previous main results remain robustly significant. Following discussions with Dr. Lynam, two clarifications of statements made in Attrill et al. (2007) are also required. Page 482, Results, last line of first column: ‘‘There were no...robust, consistent relations between jellyfish frequency and any environmental variables for B and D… contrary to the findings of previous shorter time series (Lynam et al. 2005).’’ The Lynam et al. (2004, 2005) papers presented no data for the D sector and found no link in the B sector, contrary to our revised results. Page 482, Discussion, paragraph 1, last sentence: ‘‘… positive association … North of Scotland (Lynam et al. 2005) … does not appear to be maintained.’’ Our paper did not report on any data that covered Lynam et al.’s (2005) North of Scotland area so the statement is not directly supported, although their positive relation North of Scotland, when considered in conjunction with inflow, may agree with the C2 and B2 results of Attrill et al. (2007).

Drivers of euphausiid species abundance and numerical abundance in the Atlantic Ocean

Mid-ocean ridges are common features of the world’s oceans but there is a lack of understanding as to how their presence affects overlying pelagic biota. The Mid-Atlantic Ridge (MAR) is a dominant feature of the Atlantic Ocean. Here, we examined data on euphausiid distribution and abundance arising from several international research programmes and from the continuous plankton recorder. We used a generalized additive model (GAM) framework to explore spatial patterns of variability in euphausiid distribution on, and at either side of, the MAR from 60°N to 55°S in conjunction with variability in a suite of biological, physical and environmental parameters. Euphausiid species abundance peaked in mid-latitudes and was significantly higher on the ridge than in adjacent waters, but the ridge did not influence numerical abundance significantly. Sea surface temperature (SST) was the most important single factor influencing both euphausiid numerical abundance and species abundance. Increases in sea surface height variance, a proxy for mixing, increased the numerical abundance of euphausiids. GAM predictions of variability in species abundance as a function of SST and depth of the mixed layer were consistent with present theories, which suggest that pelagic niche availability is related to the thermal structure of the near surface water: more deeply-mixed water contained higher euphausiid biodiversity. In addition to exposing present distributional patterns, the GAM framework enables responses to potential future and past environmental variability including temperature change to be explored.

In hot water: zooplankton and climate change

An overview is provided of the observed and potential future responses of zooplankton communities to global warming. I begin by describing the importance of zooplankton in ocean ecosystems and the attributes that make them sensitive beacons of climate change. Global warming may have even greater repercussions for marine ecosystems than for terrestrial ecosystems, because temperature influences water column stability, nutrient enrichment, and the degree of new production, and thus the abundance, size composition, diversity, and trophic efficiency of zooplankton. Pertinent descriptions of physical changes in the ocean in response to climate change are given as a prelude to a detailed discussion of observed impacts of global warming on zooplankton. These manifest as changes in the distribution of individual species and assemblages, in the timing of important life-cycle events, and in abundance and community structure. The most illustrative case studies, where climate has had an obvious, tangible impact on zooplankton and substantial ecosystem consequences, are presented. Changes in the distribution and phenology of zooplankton are faster and greater than those observed for terrestrial groups. Relevant projected changes in ocean conditions are then presented, followed by an exploration of potential future changes in zooplankton communities from the perspective of different modelling approaches. Researchers have used a range of modelling approaches on individual species and functional groups forced by output from climate models under future greenhouse gas emission scenarios. I conclude by suggesting some potential future directions in climate change research for zooplankton, viz. the use of richer zooplankton functional groups in ecosystem models; greater research effort in tropical systems; investigating climate change in conjunction with other human impacts; and a global zooplankton observing system.

Macro-ecology of plankton–seabird associations in the North Pacific Ocean

In conjunction with the North Pacific Continuous Plankton Recorder program, we conducted surveys of seabirds from June 2002 to June 2007. Here, we tested the hypotheses of (i) east–west variations in coupled plankton and seabird abundance, and (ii) that surface-feeding and diving seabirds vary in their relationships to primary productivity and mesozooplankton species abundance and diversity. To test these hypotheses, we developed statistical models for 20 species of seabirds and 12 zooplankton taxonomic groups. Seabird density was highly variable between seasons, but was consistently higher in the western than eastern North Pacific. Seabird diversity was greater in the east. Zooplankton abundance did not differ between regions. We found associations at the “bulk” level between seabird density and net primary productivity, but only one association between seabirds and total zooplankton abundance or diversity. However, we found many relationships between seabird species and the abundance of different zooplankton summarized at the genus or family level. Some of these taxonomic relationships reflect direct predator–prey interactions, while others may reflect zooplankton that serve as ecological indicators of other prey, such as micronekton, upon which the birds may feed. Surface or near-surface feeding, mostly piscivorous seabirds, did not differ systematically from diving, mainly planktivorous seabirds in their zooplankton associations. Seabirds apparently respond to zooplankton taxonomic groupings more so than bulk zooplankton characteristics, such as abundance or diversity. Macro-ecological studies of remote marine ecosystems using zooplankton and seabirds as ecological indicators provide a framework for understanding and assessing spatial and temporal variations in these difficult-to-study pelagic environments.

An updated climatology of surface dimethlysulfide concentrations and emission fluxes in the global ocean

The potentially significant role of the biogenic trace gas dimethylsulfide (DMS) in determining the Earth's radiation budget makes it necessary to accurately reproduce seawater DMS distribution and quantify its global flux across the sea/air interface. Following a threefold increase of data (from 15,000 to over 47,000) in the global surface ocean DMS database over the last decade, new global monthly climatologies of surface ocean DMS concentration and sea-to-air emission flux are presented as updates of those constructed 10 years ago. Interpolation/extrapolation techniques were applied to project the discrete concentration data onto a first guess field based on Longhurst's biogeographic provinces. Further objective analysis allowed us to obtain the final monthly maps. The new climatology projects DMS concentrations typically in the range of 1–7 nM, with higher levels occurring in the high latitudes, and with a general trend toward increasing concentration in summer. The increased size and distribution of the observations in the DMS database have produced in the new climatology substantially lower DMS concentrations in the polar latitudes and generally higher DMS concentrations in regions that were severely undersampled 10 years ago, such as the southern Indian Ocean. Using the new DMS concentration climatology in conjunction with state-of-the-art parameterizations for the sea/air gas transfer velocity and climatological wind fields, we estimate that 28.1 (17.6–34.4) Tg of sulfur are transferred from the oceans into the atmosphere annually in the form of DMS. This represents a global emission increase of 17% with respect to the equivalent calculation using the previous climatology. This new DMS climatology represents a valuable tool for atmospheric chemistry, climate, and Earth System models.

Indications of a climate effect on Mediterranean fisheries

Using the Food and Agriculture Organization’s (FAO) Mediterranean capture fisheries production dataset in conjunction with global and Mediterranean sea surface temperatures, we investigated trends in fisheries landings and landings per unit of effort of commercially important marine organisms, in relation to temperature oscillations. In addition to the overall warming trend, a temperature shift was detected in the Mediterranean Sea in the late 1990s. Fisheries landings fluctuations were examined for the most abundant commercial species (59 species) and showed significant year-to-year correlations with temperature for nearly 60 % of the cases. From these, the majority (~70 %) were negatively related and showed a reduction of 44 % on average. Increasing trends were found, mainly in the landings of species with short life spans, which seem to have benefited from the increase in water temperature. Τhe effect of oceanic warming is apparent in most species or groups of species sharing ecological (e.g. small and medium pelagic, demersal fish) or taxonomic (e.g. cephalopods, crustaceans) traits. A landings-per-unit-of-effort (LPUE) proxy, using data from the seven Mediterranean European Union member states, also showed significant correlation with temperature fluctuations for six out of the eight species examined, indicating the persistence of temperature influence on landings when the fishing effect is accounted for. The speed of response of marine landings to the warming of the Mediterranean Sea possibly shows both the sensitivity and the vulnerable state of the fish stocks and indicates that climate should be examined together with fisheries as a factor shaping stock fluctuations.

Genotyping an Emiliania huxleyi (Prymnesiophyceae) bloom event in the North Sea reveals evidence of asexual reproduction

Due to the unprecedented rate at which our climate is changing, the ultimate consequence for many species is likely to be either extinction or migration to an alternate habitat. Certain species might, however, evolve at a rate that could make them resilient to the effects of a rapidly changing environment. This scenario is most likely to apply to species that have large population sizes and rapid generation times, such that the genetic variation required for adaptive evolution can be readily supplied. Emiliania huxleyi (Lohm.) Hay and Mohler (Prymnesiophyceae) is likely to be such a species as it is the most conspicuous extant calcareous phytoplankton species in our oceans with generation times of 1 day−1. Here we report on a validated set of microsatellites, in conjunction with the coccolithophore morphology motif genetic marker, to genotype 93 clonal isolates collected from across the world. Of these, 52 came from a single bloom event in the North Sea collected on the D366 UK Ocean Acidification cruise in June-July 2011. There were 26 multilocus genotypes (MLGs) encountered only once in the North Sea bloom and 8 MLGs encountered twice or up to six times. Each of these repeated MLGs exhibited Psex values of less than 0.05 indicating each repeated MLG was the product of asexual reproduction and not separate meiotic events. In addition, we show that the two most polymorphic microsatellite loci, EHMS37 and P01E05, are reporting on regions likely undergoing rapid genetic drift during asexual reproduction. Despite the small sample size, there were many more repeated genotypes than previously reported for other bloom-forming phytoplankton species, including a previously genotyped E. huxleyi bloom event. This study challenges our current assumption that sex is the predominant mode of reproduction during bloom events. Whilst genetic diversity is high amongst extant populations of E. huxleyi, the root cause for this diversity and ultimate fate of these populations still requires further examination. Nonetheless, we show that certain CMM genotypes are found everywhere; while others appear to have a regional bias.

Combining metagenomics with metaproteomics and stable isotope probing reveals metabolic pathways used by a naturally occurring marine methylotroph

A variety of culture-independent techniques have been developed that can be used in conjunction with culture-dependent physiological and metabolic studies of key microbial organisms, in order to better understand how the activity of natural populations influences and regulates all major biogeochemical cycles. In this study, we combined DNA-stable isotope probing with metagenomics and metaproteomics to characterize an as yet uncultivated marine methylotroph that actively incorporated carbon from 13C-labeled methanol into biomass. By metagenomic sequencing of the heavy DNA, we retrieved virtually the whole genome of this bacterium and determined its metabolic potential. Through protein-stable isotope probing, the RuMP cycle was established as the main carbon assimilation pathway, and the classical methanol dehydrogenase-encoding gene mxaF, as well as three out of four identified xoxF homologues were found to be expressed. This proof-of-concept study is the first in which theculture-independent techniques of DNA- and protein-stable isotope probing have been used to characterize the metabolism of a naturally-ocurring Methylophaga-like bacterium in the marine environment (i.e. M. thiooxydans L4) and thus provides a powerful approach to access the genome and proteome of uncultivated microbes involved in key processes in the environment

Prioritization of knowledge needs for sustainable aquaculture: a national and global perspective

Aquaculture is currently the fastest expanding global animal food production sector and is a key future contributor to food security. An increase in food security will be dependent upon the development and improvement of sustainable practices. A prioritization exercise was undertaken, focusing on the future knowledge needs to underpin UK sustainable aquaculture (both domestic and imported products) using a ‘task force’ group of 36 ‘practitioners’ and 12 ‘research scientists’ who have an active interest in sustainable aquaculture. A long list of 264 knowledge needs related to sustainable aquaculture was developed in conjunction with the task force. The long list was further refined through a three stage process of voting and scoring, including discussions of each knowledge need. The top 25 knowledge needs are presented, as scored separately by ‘practitioners’ or ‘research scientists’. There was similar agreement in priorities identified by these two groups. The priority knowledge needs will provide guidance to structure ongoing work to make science accessible to practitioners and help to prioritize future science policy needs and funding. The process of knowledge exchange, and the mechanisms by which this can be achieved, effectively emerged as the top priority for sustainable aquaculture. Viable alternatives to wild fish-based aquaculture feeds, resource constraints that will potentially limit expansion of aquaculture, sustainable offshore aquaculture and the treatment of sea lice also emerged as strong priorities. Although the exercise was focused on UK needs for sustainable aquaculture, many of the emergent issues are considered to have global application.