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).

Plankton populations at the bifurcation of the North Pacific Current

As the eastward-flowing North Pacific Current approaches the North American continent it bifurcates into the southward-flowing California Current and the northward-flowing Alaska Current. This bifurcation occurs in the south-eastern Gulf of Alaska and can vary in position. Dynamic height data from Project Argo floats have recently enabled the creation of surface circulation maps which show the likely position of the bifurcation; during 2002 it was relatively far north at 53 degrees N then, during early 2003, it moved southwards to a more normal position at 45 degrees N. Two ship-of-opportunity transects collecting plankton samples with a Continuous Plankton Recorder across the Gulf of Alaska were sampled seasonally during 2002 and 2003. Their position was dependent on the commercial ship's operations; however, most transects sampled across the bifurcation. We show that the oceanic plankton differed in community composition according to the current system they occurred in during spring and fall of 2002 and 2003, although winter populations were more mixed. Displacement of the plankton communities could have impacts on the plankton's reproduction and development if they use cues such as day length, and also on foraging of higher trophic-level organisms that use particular regions of the ocean if the nutritional value of the communities is different. Although we identify some indicator taxa for the Alaska and California currents, functional differences in the plankton communities on either side of the bifurcation need to be better established to determine the impacts of bifurcation movement on the ecosystems of the north-east Pacific.

Shortened duration of the annual Neocalanus plumchrus biomass peak in the Northeast Pacific

The calanoid copepod Neocalan us plumchrus (Marukawa) is a dominant member of the spring mesozooplankton in the subarctic North Pacific and Bering Sea. Previous studies have shown interdecadal and latitudinal variation in seasonal developmental timing, with peak biomass occurring earlier in years and places with warmer upper ocean temperatures. Because N. plumchrus normally has a single dominant annual cohort, its seasonal timing can be indexed from measurements of total population biomass or by following progressive changes in stage composition. Early studies empirically found that peak upper ocean biomass occurred when about half of the pre-dormant population had reached copepodite stage 5 (C5). However, more recent comparisons derived from recent Continuous Plankton Recorder (CPR) data now show peak biomass when a larger fraction (> 80%) of the population is at C5. CPR samples the surface 10 to 15 m, but comparisons to depth-resolved BIONESS data show that this discrepancy is not an artefact of sampling depth. Other causes are either a prolongation of duration of pre-dormant C5 or a narrowing of the age range making up the annual cohort. We assessed changes in cohort width using a modification of Greve's cumulative percentile method, and found that average cohort widths in the Alaska Gyre were significantly narrower in 2000-2007 than in 1957-1965 (1968-1980 were intermediate). Net tow sampling of Strait of Georgia populations showed a similar significant narrowing of cohorts in the 2003-2005 sampling period. This study provides evidence that in addition to the shift to an earlier occurrence of peak biomass reported previously, the duration of the peak has also decreased in the last decade.

Simple procedures to assess and compare the ecological niche of species

Hutchinson's (1957; Cold Spring Harbour Symp Quant Biol 22:415-427) niche concept is being used increasingly in the context of global change, and is currently applied to many ecological issues including climate change, exotic species invasion and management of endangered species. For both the marine and terrestrial realms, there is a growing need to assess the breadth of the niches of individual species and to make comparisons among them to forecast the species' capabilities to adapt to global change. In this paper, we describe simple non-parametric multivariate procedures derived from a method originally used in climatology to (1) evaluate the breadth of the ecological niche of a species and (2) examine whether the niches are significantly separated. We first applied the statistical procedures to a simple fictive example of 3 species separated by 2 environmental factors in order to describe the technique. We then used it to quantify and compare the ecological niche of 2 key-structural marine zooplankton copepod species, Calanus finmarchicus and C. helgolandicus, in the northern part of the North Atlantic Ocean using 3 environmental factors. The test demonstrates that the niches of both species are significantly separated and that the coldwater species has a niche larger than that of its warmer-water congeneric species.

On the processes linking climate to ecosystem changes

While documentation of climate effects on marine ecosystems has a long history, the underlying processes have often been elusive. In this paper we review some of the ecosystem responses to climate variability and discuss the possible mechanisms through which climate acts. Effects of climatological and oceanographic variables, such as temperature, sea ice, turbulence, and advection, on marine organisms are discussed in terms of their influence on growth, distribution, reproduction, activity rates, recruitment and mortality. Organisms tend to be limited to specific thermal ranges with experimental findings showing that sufficient oxygen supply by ventilation and circulation only occurs within these ranges. Indirect effects of climate forcing through effects on the food web are also discussed. Research and data needs required to improve our knowledge of the processes linking climate to ecosystem changes are presented along with our assessment of our ability to predict ecosystem responses to future climate change scenarios. (C) 2009 Elsevier B.V. All rights reserved.

Southern Ocean biogeography and taxonomic resolution: what's in the name?

We examined the taxonomic resolution of zooplankton data required to identify ocean basin scale biogeographic zonation in the Southern Ocean. A 2,154 km transect was completed south of Australia. Sea surface temperature (SST) measured at 1 min intervals showed that seven physical zones were sampled. Zooplankton were collected at a spatial resolution of similar to 9.2 km with a continuous plankton recorder, identified to the highest possible taxonomic resolution and enumerated. Zooplankton assemblage similarity between samples was calculated using the Bray-Curtis index for the taxonomic levels of species, genus, family, order and class after first log(10)(x + 1) (LA) and then presence/absence (PA) transformation of abundance data. Although within and between zone sample similarity increased with decreasing taxonomic resolution, for both data transformations, cluster analysis demonstrated that the biogeographic separation of zones remained at all taxonomic levels when using LA data. ANOSIM confirmed this, detecting significant differences in zooplankton assemblage structure between all seven a priori determined physical zones for all taxonomic levels when using the LA data. In the case of the PA data for the complete data set, and both LA and PA data for a crustacean only data set, no significant differences were detected between zooplankton assemblages in the Polar frontal zone (PFZ) and inter-PFZ at any taxonomic level. Loss of information at resolutions below the species level, particularly in the PA data, prevented the separation of some zones. However, the majority of physical zones were biogeographically distinct from species level to class using both LA and PA transformations. Significant relationships between SST and zooplankton community structure, summarised as NMDS scores, at all taxonomic levels, for both LA and PA transformations, and complete and crustacean only data sets, highlighted the biogeographic relevance of low resolution taxonomic data. The retention of biogeographic information in low taxonomic resolution data shows that data sets collected with different taxonomic resolutions may be meaningfully merged for the post hoc generation of Southern Ocean time series.

Indications of a negative impact of herring on recruitment of Norway pout

The Norway pout (Trisopterus esmarkii) stock in the North Sea has experienced poor recruitment recently. Herring (Clupea harengus) has been suggested to be a major predator on fish larvae in the North Sea. We investigated possible interactions between herring and Norway pout using a simple statistical analysis and a modified stock - recruit relationship. There was a significant negative relationship (linear regression, r = 20.44, p < 0.05) between total herring biomass and recruitment of Norway pout. The spawning stock of Norway pout is typically dominated by 2-year-olds, and there was a strong negative relationship (linear regression, r = 20.79, p < 0.01) between herring biomass and Norway pout spawning-stock biomass (SSB) 2 years later. A Beverton-Holt model fitted to stock recruit data of Norway pout produced a rather poor correlation (r(2) = 0.04). However, when only the Norway pout SSB not overlapping with herring is considered, the fit between the model and the stock - recruit data improves (r(2) = 0.31). The analyses indicate a negative impact by herring on recruitment of Norway pout, the most plausible cause for this being herring predation on Norway pout larvae, but field studies are needed to verify such predation.

Monitoring marine plankton ecosystems: Identification of the most relevant indicators of the state of an ecosystem

The number of variables involved in the monitoring of an ecosystem can be high and often one of the first stages in the analysis is to reduce the number of variables. We describe a method developed for geological purposes, using the information theory, that enables selection of the most relevant variables. This technique also allows the examination of the asymmetrical relationships between variables. Applied to a set of physical and biological variables (plankton assemblages in four areas of the North Sea), the method shows that biological variables are more informative than physical variables although the controlling factors are mainly physical (sea surface temperature in winter and spring). Among biological variables, diversity measures and warm-water species assemblages are informative for the state of the North Sea pelagic ecosystems while among physical variables sea surface temperature in late winter and early spring are highly informative. Although often used in bioclimatology, the utilisation of the North Atlantic Oscillation (NAO) index does not seem to provide a lot of information. The method reveals that only the extreme states of this index has an influence on North Sea pelagic ecosystems. The substantial and persistent changes that were detected in the dynamic regime of the North Sea ecosystems and called regime shift are detected by the method and corresponds to the timing of other shifts described in the literature for some European Systems such as the Baltic and the Mediterranean Sea when both physical and biological variables are considered.

Distribution and multi-annual abundance trends of the copepod Temora longicornis in the US Northeast shelf ecosystem

The average spatial distribution and annual abundance cycle are described for the copepod Temora longicornis from samples collected on broadscale surveys (1977-2006) and along continuous plankton recorder transects (1961-2006) of the US Northeast continental shelf ecosystem. After its annual low in winter, T. longicornis abundance begins to increase in coastal waters with the northern progression of spring conditions. Annual maximum shelf concentrations were found in the more southern inshore waters of the region during the summer months. Abundance throughout most of the ecosystem increased sharply in the early 1990s and remained high through 2001. During this period, the copepod became more numerous and widespread in offshore shelf waters. Abundance declined to approximately average levels in 2002 for the remainder of the time series, but its extended offshore range remained intact. Correlation analysis found that the copepods interannual abundance variability had a significant negative relationship with surface salinity anomalies throughout the ecosystem, with higher correlations found in the northernmost subareas. Temora longicornis abundance in the ecosystem's southernmost subarea (Middle Atlantic Bight) did not increase in the 1990s and was found to be negatively correlated to surface temperature, indicating that continued global warming could adversely impact the copepods annual abundance cycle in this region.

Trophic amplification of climate warming

Ecosystems can alternate suddenly between contrasting persistent states due to internal processes or external drivers. It is important to understand the mechanisms by which these shifts occur, especially in exploited ecosystems. There have been several abrupt marine ecosystem shifts attributed either to fishing, recent climate change or a combination of these two drivers. We show that temperature has been an important driver of the trophodynamics of the North Sea, a heavily fished marine ecosystem, for nearly 50 years and that a recent pronounced change in temperature established a new ecosystem dynamic regime through a series of internal mechanisms. Using an end-to-end ecosystem approach that included primary producers, primary, secondary and tertiary consumers, and detritivores, we found that temperature modified the relationships among species through nonlinearities in the ecosystem involving ecological thresholds and trophic amplifications. Trophic amplification provides an alternative mechanism to positive feedback to drive an ecosystem towards a new dynamic regime, which in this case favours jellyfish in the plankton and decapods and detritivores in the benthos. Although overfishing is often held responsible for marine ecosystem degeneration, temperature can clearly bring about similar effects. Our results are relevant to ecosystem-based fisheries management (EBFM), seen as the way forward to manage exploited marine ecosystems.

Climate-induced effects on the meroplankton and the benthic-pelagic ecology of the North Sea

Analyses of long-term time series of North Sea plankton and sea surface temperature (SST) data reveal that the annual planktonic larval abundance of three benthic phyla, Echinodermata, Arthropoda, and Mollusca, responds positively and immediately to SST. Long-term outcomes for the planktonic abundance of these three phyla are different, however. The planktonic larvae of echinoderms and decapod crustaceans have increased in abundance from 1958 to 2005, and especially since the mid-1980s, as North Sea SST has increased. In contrast, the abundance of bivalve mollusc larvae has declined, despite the positive year-to-year relationship between temperature and bivalve larval abundance continuing to hold. We argue that the changes in meroplankton abundance, coincident with increased phytoplankton and declining holoplankton, reflect the synchronous effect of rising SST and related changes in the pelagic community on the reproduction and recruitment of many benthic marine invertebrates. Under this scenario, the long-term decline in bivalve mollusc larvae will reflect increased predation on the settled larvae and adults by benthic decapods. These alterations in the zooplankton may therefore describe an ecosystem-wide restructuring of North Sea trophic interactions.

Decadal fluctuations in North Atlantic water inflow in the North Sea between 1958-2003: impacts on temperature and phytoplankton populations

The circulation of Atlantic water along the European continental slope, in particular the inflow into the North Sea, influences North Sea water characteristics with consequent changes in the environment affecting plankton community dynamics. The long-term effect of fluctuating oceanographic conditions oil the North Sea, pelagic ecosystem is assessed. It is shown that (i) there are similar regime shifts in the inflow through the northern North Sea and in Sea, Surface Temperature, (ii) long-term phytoplankton trends are influenced by the inflow only in some North Sea regions, and (iii) the spatial variability in chemicophysical and biological parameters highlight the influence of smaller scale processes.

Effects on zooplankton of a warmer ocean: Recent evidence from the Northeast Pacific

The consequences for pelagic communities of warming trends in mid and high latitude ocean regions could be substantial, but their magnitude and trajectory are not yet known. Environmental changes predicted by climate models (and beginning to be confirmed by observations) include warming and freshening of the upper ocean and reduction in the extent and duration of ice cover. One way to evaluate response scenarios is by comparing how "similar" zooplankton communities have differed among years and/or locations with differing temperature. The subarctic Pacific is a strong candidate for such comparisons, because the same mix of zooplankton species dominates over a wide range of temperature climatologies, and observations have spanned substantial temperature variability at interannual-to-decadal time scales. In this paper, we review and extend copepod abundance and phenology time series from net tow and Continuous Plankton Recorder surveys in the subarctic Northeast Pacific. The two strongest responses we have observed are latitudinal shifts in centers of abundance of many species (poleward under warm conditions), and changes in the life cycle timing of Neocalanus plumchrus in both oceanic and coastal regions (earlier by several weeks in warm years and at warmer locations). These zooplankton data, plus indices of higher trophic level responses such as reproduction, growth and survival of pelagic fish and seabirds, are all moderately-to-strongly intercorrelated (vertical bar r vertical bar = 0.25-0.8) with indices of local and basin-scale temperature anomalies. A principal components analysis of the normalized anomaly time series from 1979 to 2004 shows that a single "warm-and-low-productivity" vs. "cool-and-high-productivity" component axis accounts for over half of the variance/covariance. Prior to 1990, the scores for this component were negative ("cool" and "productive") or near zero except positive in the El Nino years 1983 and 1987. The scores were strongly and increasingly positive ("warm" and "low productivity") from 1992 to 1998; negative from 1999 to 2002; and again increasingly positive from 2003-present. We suggest that, in strongly seasonal environments, anomalously high temperature may provide misleading environmental cues that contribute to timing mismatch between life history events and the more-nearly-fixed seasonality of insolation, stratification, and food supply. Crown Copyright (c) 2007 Published by Elsevier Ltd. All rights reserved.

Zooplankton response to a warmer northern Wadden Sea

Weekly measurements of mesozooplankton (>76 mu m) and hydrographic parameters have been carried out since 1984 in the List Tidal Basin (northern Wadden Sea). Monthly water temperature significantly increased by 0.04 degrees C year. The largest increase by 3 degrees C in 22 years occurred in September, implying, an extension of the warm summer period. Mean annual copepod abundance and length of copepod season correlated significantly with mean temperature from January to May. Except for an increasing Acartia sp. abundance during spring (April-May), no longterm trends in copepod abundance were observed. The percentage of carnivorous zooplankton increased significantly since 1984 mainly due to a sudden increase in the cyclopoid copepod Oithona similis in 1997. We expect that global warming will lead to a longer copepod season and higher copepod abundances in the northern Wadden Sea.

Microbial spatial variability: An example from the Celtic Sea

In July 2004, dominant populations of microbial ultraplankton (<5 μm), in the surface of the Celtic Sea (between UK and Eire), were repeatedly mapped using flow cytometry, at 1.5 km resolution over a region of diameter 100 km. The numerically dominant representatives of all basic functional types were enumerated including one group of phototrophic bacteria (Syn), two groups of phytoplankton (PP, NP), three groups of heterotrophic bacterioplankton (HB) and the regionally dominant group of heterotrophic protists (HP). The distributions of all organisms showed strong spatial variability with little relation to variability in physical fields such as salinity and temperature. Furthermore, there was little agreement between distributions of different organisms. The only linear correlation consistently explaining more than 50% of the variance between any pairing of the organism groups enumerated is between two different groups of HB. Specifically, no linear, or non-linear, relationship is found between any pairings of SYB, PP or HB groups with their protist predators HP. Looking for multiple dependencies, factor analysis reveals three groupings: Syn, PP and low nucleic acid content HB (LNA); high nucleic acid content HB (HNA); HP and NP. Even the manner in which the spatial variability of Syn, PP and HB abundance varies as a function of lengthscale (represented by a semivariogram) differs significantly from that for HP. In summary, although all microbial planktonic groups enumerated are present and numerically dominant throughout the region studied, at face value the relationships between them seem weak. Nevertheless, the behaviour of a simple, illustrative ecological model, with strongly interacting phototrophs and heterotrophs, with stochastic forcing, is shown to be consistent with the observed poor correlations and differences in how spatial variability varies with lengthscale. Thus, our study suggests that a comparison of microbial abundances alone may not discern strong underlying trophic interactions. Specific knowledge of these processes, in particular grazing, will be required to explain the causes of the observed microbial spatial variability and its resulting consequences for the functioning of the ecosystem.