Marine plankton phenology and life history in a changing climate: current research and future directions

Increasing availability and extent of biological ocean time series (from both in situ and satellite data) have helped reveal significant phenological variability of marine plankton. The extent to which the range of this variability is modified as a result of climate change is of obvious importance. Here we summarize recent research results on phenology of both phytoplankton and zooplankton. We suggest directions to better quantify and monitor future plankton phenology shifts, including (i) examining the main mode of expected future changes (ecological shifts in timing and spatial distribution to accommodate fixed environmental niches vs. evolutionary adaptation of timing controls to maintain fixed biogeography and seasonality), (ii) broader understanding of phenology at the species and community level (e.g. for zooplankton beyond Calanus and for phytoplankton beyond chlorophyll), (iii) improving and diversifying statistical metrics for indexing timing and trophic synchrony and (iv) improved consideration of spatio-temporal scales and the Lagrangian nature of plankton assemblages to separate time from space changes.

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.

Synergistic effects of climate and fishing in a marine ecosystem

Current climate change and overfishing are affecting the productivity and structure of marine ecosystems. This situation is unprecedented for the marine biosphere and it is essential to understand the mechanisms and pathways by which ecosystems respond. We report that climate change and overfishing are likely to be responsible for a rapid restructuring of a highly productive marine ecosystem with effects throughout the pelagos and the benthos. In the mid-1980s, climate change, consequent modifications in the North Sea plankton, and fishing, all reduced North Sea cod recruitment. In this region, production of many benthic species respond positively and immediately to temperature. Analysis of a long-term, spatially extensive biological (plankton and cod) and physical (sea surface temperature) dataset suggests that synchronous changes in cod numbers and sea temperature have established an extensive trophic cascade favoring lower trophic level groups over economic fisheries. A proliferation of jellyfish that we detect may signal the climax of these changes. This modified North Sea ecology may provide a clear indication of the synergistic consequences of coincident climate change and overfishing. The extent of the ecosystem restructuring that has occurred in the North Sea suggests we are unlikely to reverse current climate and human-induced effects through ecosystem resource management in the short term. Rather, we should understand and adapt to new ecological regimes. This implies that fisheries management policies will have to be fully integrated with the ecological consequences of climate change to prevent a similar collapse in an exploited marine ecosystem elsewhere.

Climate-induced changes in the North Sea Decapoda over the last 60 years

In the mid-1980s the North Sea ecosystem experienced a climate-induced regime shift that has favoured decapods and detritivores in the benthos and jellyfish in the plankton over commercial fisheries. Here, we investigate changes among the Decapoda in the North Sea plankton over the last 60 yr. Decapods are important predators in the plankton and the benthos where they can influence productivity and structure communities. In the North Sea it has been suggested that a climate-driven increase in decapod abundance has been important in propagating the climate signal through the North Sea food web. We show that climate-induced changes in the Decapoda in the central and southern North Sea include the presence of new warm-water taxa, changes in the abundance and proportions of commercial species of shrimp, and an earlier occurrence of decapod larvae in the plankton compared with the period 1981–1983. Notable amongst the warm-water taxa appearing in the North Sea is the predatory swimming crab Polybius henslowii that can swarm in large numbers when conditions are favourable and that is known to exhibit range shifts in response to fluctuations in hydroclimatic forcing. We suggest that climate-induced changes among North Sea decapods have played an important role in the trophic amplification of a climate signal and the development of the new North Sea dynamic regime. Understanding these changes is likely to be imperative for a successful ecosystem-based approach to the future management of North Sea fisheries at a time of climate change.

North Sea ecosystem change from swimming crabs to seagulls

A recent increase in sea temperature has established a new ecosystem dynamic regime in the North Sea. Climate-induced changes in decapods have played an important role. Here, we reveal a coincident increase in the abundance of swimming crabs and lesser black-backed gull colonies in the North Sea, both in time and in space. Swimming crabs are an important food source for lesser black-backed gulls during the breeding season. Inhabiting the land, but feeding mainly at sea, lesser black-backed gulls provide a link between marine and terrestrial ecosystems, since the bottom-up influence of allochthonous nutrient input from seabirds to coastal soils can structure the terrestrial food web. We, therefore, suggest that climate-driven changes in trophic interactions in the marine food web may also have ensuing ramifications for the coastal ecology of the North Sea.

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.

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.

Zooplankton associations in a Mediterranean long-term time-series

Coastal zooplankton have been investigated since 1984 at a Long Term Ecological Research station MC (LTER-MC) in the inner Gulf of Naples (Tyrrhenian Sea, Western Mediterranean). The sampling site, located between the littoral and the open sea systems, has very active hydrography that affects plankton communities. The present work was aimed at establishing whether, in such a dynamic and variable environment, species associations and homogeneous periods could be identified as characteristic and stable features of the mesozooplankton over the period 1984–2006. Hierarchical clustering was applied to assess species associations based on a matrix of similarities between species (R-mode), and homogeneous periods based on a matrix of similarities between observations (Q-mode). The Indicator Value index [IndVal, Dufrene and Legendre (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol. Monogr., 67, 345–366] was calculated to identify species characterizing each period. Five taxonomic groups with well-defined composition and abundance were identified as robust associations that likely reflect different modes of community functioning. The temporal course of these associations was largely shaped by strong seasonal forcing comprising both physical and biological (e.g. trophic) signals. These associations persisted over the long term, thus indicating some stable characters in the Naples zooplankton time-series, providing evidence of resilience in communities in highly variable coastal conditions.

Trophodynamics and stability of regional scale ecosystems in the Northeast Atlantic

This study addresses the long-term stability of three trophic groupings in the Northeast Atlantic at regional scales. The most abundant taxa representing phytoplankton, herbivorous copepods, and carnivorous zooplankton were examined from the Continuous Plankton Recorder database. Multivariate control charts using a Bray–Curtis similarity metric were used to assess whether fluctuations within trophic groupings were within or beyond the expected variability. Two evaluation periods were examined: annual changes between 1960 and 1999 (2000–2009 baseline) and recent changes between 2000 and 2009 (1960–1999 baseline). The trends over time in abundance/biomass of trophic levels were region-specific, especially in carnivorous copepods, where abundance did not mirror trends in the overall study area. The stability of phytoplankton was within the expected limits, although not in 2008 and 2009. Higher trophic levels were less stable, perhaps reflecting the added complexity of interactions governing their abundance. In addition, some regions were consistently less stable than others. Correlations in stability between adjacent trophic levels were positive at large marine ecosystem scale but generally non-significant at regional scales. The study suggests that certain regions may be particularly vulnerable to periods of instability in community structure. The benefits of using the control chart method rather than other multivariate measures of plankton dynamics are discussed.

Is there a decline in marine phytoplankton?

Phytoplankton account for approximately 50% of global primary production, form the trophic base of nearly all marine ecosystems, are fundamental in trophic energy transfer and have key roles in climate regulation, carbon sequestration and oxygen production. Boyce et al.1 compiled a chlorophyll index by combining in situ chlorophyll and Secchi disk depth measurements that spanned a more than 100-year time period and showed a decrease in marine phytoplankton biomass of approximately 1% of the global median per year over the past century. Eight decades of data on phytoplankton biomass collected in the North Atlantic by the Continuous Plankton Recorder (CPR) survey2, however, show an increase in an index of chlorophyll (Phytoplankton Colour Index) in both the Northeast and Northwest Atlantic basins3, 4, 5, 6, 7 (Fig. 1), and other long-term time series, including the Hawaii Ocean Time-series (HOT)8, the Bermuda Atlantic Time Series (BATS)8 and the California Cooperative Oceanic Fisheries Investigations (CalCOFI)9 also indicate increased phytoplankton biomass over the last 20–50 years. These findings, which were not discussed by Boyce et al.1, are not in accordance with their conclusions and illustrate the importance of using consistent observations when estimating long-term trends.

Recruitment in a changing environment: the 2000s North Sea herring recruitment failure

Environmentally induced change appears to be impacting the recruitment of North Sea herring (Clupea harengus). Despite simultaneously having a large adult population, historically low exploitation, and Marine Stewardship Council accreditation (implying sustainability), there have been an unprecedented 6 sequential years of poor juvenile production (recruitment). Analysis suggests that the poor recruitment arises during the larval overwintering phase, with recent survival rates greatly reduced. Contemporary warming of the North Sea has caused significant changes in the plankton community, and a recently identified regime shift around 2000 shows close temporal agreement with the reduced larval survival. It is, therefore, possible that we are observing the first consequences of this planktonic change for higher trophic levels. There is no indication of a recovery in recruitment in the short term. Fishing mortality is currently outside the agreed management plan, and forecasts show a high risk of the stock moving outside safe biological limits soon, potentially precipitating another collapse of the stock. However, bringing the realized fishing mortality back in line with the management plan would likely alleviate the problem. This illustrates again that recruitment is influenced by more than just spawning-stock biomass, and that changes in other factors can be of equal, or even greater, importance. In such dynamically changing environments, recent management success does not necessarily guarantee future sustainability.

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.

Global latitudinal variations in marine copepod diversity and environmental factors

Latitudinal gradients in diversity are among the most striking features in ecology. For terrestrial species, climate (i.e. temperature and precipitation) is believed to exert a strong influence on the geographical distributions of diversity through its effects on energy availability. Here, we provide the first global description of geographical variation in the diversity of marine copepods, a key trophic link between phytoplankton and fish, in relation to environmental variables. We found a polar-tropical difference in copepod diversity in the Northern Hemisphere where diversity peaked at subtropical latitudes. In the Southern Hemisphere, diversity showed a tropical plateau into the temperate regions. This asymmetry around the Equator may be explained by climatic conditions, in particular the influence of the Inter-Tropical Convergence Zone, prevailing mainly in the northern tropical region. Ocean temperature was the most important explanatory factor among all environmental variables tested, accounting for 54 per cent of the variation in diversity. Given the strong positive correlation between diversity and temperature, local copepod diversity, especially in extra-tropical regions, is likely to increase with climate change as their large-scale distributions respond to climate warming.

Temporal change in UK marine communities: trends or regime shifts?

A regime shift is a large, sudden, and long-lasting change in the dynamics of an ecosystem, affecting multiple trophic levels. There are a growing number of papers that report regime shifts in marine ecosystems. However, the evidence for regime shifts is equivocal, because the methods used to detect them are not yet well developed. We have collated over 300 biological time series from seven marine regions around the UK, covering the ecosystem from phytoplankton to marine mammals. Each time series consists of annual measures of abundance for a single group of organisms over several decades. We summarised the data for each region using the first principal component, weighting either each time series or each biological component (e.g. plankton, fish, benthos) equally. We then searched for regime shifts using Rodionov’s regime shift detection (RSD) method, which found regime shifts in the first principal component for all seven marine regions. However, there are consistent temporal trends in the data for six of the seven regions. Such trends violate the assumptions of RSD. Thus, the regime shifts detected by RSD in six of the seven regions are likely to be artefacts caused by temporal trends. We are therefore developing more appropriate time series models for both single populations and whole communities that will explicitly model temporal trends and should increase our ability to detect true regime shift events.

Black-legged kittiwakes as indicators of environmental change in the North Sea; evidence from long-term studies

Top predators, particularly seabirds, have repeatedly been suggested as indicators of marine ecosystem status. One region currently under pressure from human fisheries and climate change is the North Sea. Standardized seabird monitoring data have been collected on the Isle of May, an important seabird colony in the northwestern North Sea, over the last 10–20 years. Over this period oceanographic conditions have varied markedly, and between 1990 and 1999 a major industrial fishery for sandlance (Ammodytes marinus), the main prey of most seabird species, was prosecuted nearby. Sandlance fishing grounds close to seabird colonies down the east coast of the UK were closed in 2000 in an attempt to improve foraging opportunities for breeding seabirds, particularly black-legged kittiwakes (Rissa tridactyla). Initially this closure seemed to be beneficial for kittiwakes with breeding success recovering to pre-fishery levels. However, despite the ban continuing, kittiwakes and many other seabird species in the North Sea suffered severe breeding failures in 2004. In this paper, we test the predictive power of four previously established correlations between kittiwake breeding success and climatic/trophic variables to explain the observed breeding success at the Isle of May in 2004. During the breeding season, kittiwakes at this colony switch from feeding on 1+ group to 0 group sandlance, and results up until 2003 indicated that availability of both age classes had a positive effect on kittiwake breeding success. The low breeding success of kittiwakes in 2004 was consistent with the late appearance and small body size of 0 group sandlance, but at odds with the two variables likely to operate via 1 group availability (lagged winter sea surface temperature and larval sandlance cohort strength in 2003). The reason for the discrepancy is currently unknown, but analysis of 1 group sandlance body composition indicated that lipid content in 2004 was extremely low, and thus fish eaten by kittiwakes during pre-breeding and early incubation were likely to be of poor quality. Monitoring of reproductive success of kittiwakes, although useful, was clearly not sufficient to tease apart the complex causation underlying the 2004 event. Monitoring programs such as this, therefore, need to be complemented by detailed research to identify the mechanisms involved, and to attribute and predict the effects of natural and human-induced environmental change.