Phenological trends and trophic mismatch across multiple levels of a North Sea pelagic food web

Differential phenological responses to climate among species are predicted to disrupt trophic interactions, but datasets to evaluate this are scarce. We compared phenological trends for species from 4 levels of a North Sea food web over 24 yr when sea surface temperature (SST) increased significantly. We found little consistency in phenological trends between adjacent trophic levels, no significant relationships with SST, and no significant pairwise correlations between predator and prey phenologies, suggesting that trophic mismatching is occurring. Finer resolution data on timing of peak energy demand (mid-chick-rearing) for 5 seabird species at a major North Sea colony were compared to modelled daily changes in length of 0-group (young of the year) lesser sandeels Ammodytes marinus. The date at which sandeels reached a given threshold length became significantly later during the study. Although the phenology of all the species except shags also became later, these changes were insufficient to keep pace with sandeel length, and thus mean length (and energy value) of 0-group sandeels at mid-chick-rearing showed net declines. The magnitude of declines in energy value varied among the seabirds, being more marked in species showing no phenological response (shag, 4.80 kJ) and in later breeding species feeding on larger sandeels (kittiwake, 2.46 kJ) where, due to the relationship between sandeel length and energy value being non-linear, small reductions in length result in relatively large reductions in energy. However, despite the decline in energy value of 0-group sandeels during chick-rearing, there was no evidence of any adverse effect on breeding success for any of the seabird species. Trophic mismatch appears to be prevalent within the North Sea pelagic food web, suggesting that ecosystem functioning may be disrupted.

Trophic level asynchrony in rates of phenological change for marine, freshwater and terrestrial environments

Recent changes in the seasonal timing (phenology) of familiar biological events have been one of the most conspicuous signs of climate change. However, the lack of a standardized approach to analysing change has hampered assessment of consistency in such changes among different taxa and trophic levels and across freshwater, terrestrial and marine environments. We present a standardized assessment of 25 532 rates of phenological change for 726 UK terrestrial, freshwater and marine taxa. The majority of spring and summer events have advanced, and more rapidly than previously documented. Such consistency is indicative of shared large scale drivers. Furthermore, average rates of change have accelerated in a way that is consistent with observed warming trends. Less coherent patterns in some groups of organisms point to the agency of more local scale processes and multiple drivers. For the first time we show a broad scale signal of differential phenological change among trophic levels; across environments advances in timing were slowest for secondary consumers, thus heightening the potential risk of temporal mismatch in key trophic interactions. If current patterns and rates of phenological change are indicative of future trends, future climate warming may exacerbate trophic mismatching, further disrupting the functioning, persistence and resilience of many ecosystems and having a major impact on ecosystem services.

Live discrimination of Calanus glacialis and C. finmarchicus females: can we trust phenological differences?

Two key players in the Arctic and subarctic marine ecosystem are the calanoid copepods, Calanus finmarchicus and C. glacialis. Although morphologically very similar, these sibling species have different life cycles and roles in the Arctic pelagic marine ecosystem. Considering that the distribution of C. glacialis corresponds to Arctic water masses and C. finmarchicus to Atlantic water masses, the species are frequently used as climate indicators. Consequently, correct identification of the two species is essential if we want to understand climate-impacted changes on Calanus-dominated marine ecosystems such as the Arctic. Here, we present a novel morphological character (redness) to distinguish live females of C. glacialis and C. finmarchicus and compare it to morphological (prosome length) and genetic identification. The characters are tested on 300 live females of C. glacialis and C. finmarchicus from Disko Bay, western Greenland. Our analysis confirms that length cannot be used as a stand-alone criterion for separation. The results based on the new morphological character were verified genetically using a single mitochondrial marker (16S) and nuclear loci (six microsatellites and 12 InDels). The pigmentation criterion was also used on individuals (n = 89) from Young Sound fjord, northeast Greenland to determine whether the technique was viable in different geographical locations. Genetic markers based on mitochondrial and nuclear loci were corroborative in their identification of individuals and revealed no hybrids. Molecular identification confirmed that live females of the two species from Greenlandic waters, both East and West, can easily be separated by the red pigmentation of the antenna and somites of C. glacialis in contrast to the pale opaque antenna and somites of C. finmarchicus, confirming that the pigmentation criterion is valid for separation of the two species

Impact of climate change on marine pelagic phenology and trophic mismatch

Phenology, the study of annually recurring life cycle events such as the timing of migrations and flowering, can provide particularly sensitive indicators of climate change. Changes in phenology may be important to ecosystem function because the level of response to climate change may vary across functional groups and multiple trophic levels. The decoupling of phenological relationships will have important ramifications for trophic interactions, altering food-web structures and leading to eventual ecosystem-level changes. Temperate marine environments may be particularly vulnerable to these changes because the recruitment success of higher trophic levels is highly dependent on synchronization with pulsed planktonic production. Using long-term data of 66 plankton taxa during the period from 1958 to 2002, we investigated whether climate warming signals are emergent across all trophic levels and functional groups within an ecological community. Here we show that not only is the marine pelagic community responding to climate changes, but also that the level of response differs throughout the community and the seasonal cycle, leading to a mismatch between trophic levels and functional groups.

Ecological Status Report: results from the CPR Survey 2004/2005.

Using a number of ecological indices, this report summarises unusual species found, large phytoplankton blooms, changes in community structure and trends in hydrobiological indicators from regions in the North Atlantic (with an emphasis on the North Sea). In the majority of cases the term unuasual or large in referring to phytoplankton blooms refers to population increases greater than four standard deviations above the species recorded baseline mean (baseline mean: 1980-2003). Notable blooms that are geographically lareg refer to patch sizes greater then 100 km in diameter. The primary regional assessment area used to monitor changes in community structure, biomass and phenological changes is the central North Sea. Most data analysis has been performed to highlight the year 2004 in relation to the long-term dataset. 2005 sample data is presented but has not yet undergone quality checks. Annual abundance estimates were calculated for each CPR box when eight or more months were sampled, no annual estimate of abundance was calculated. Sea surface temperature was used as an indicator of ocean climate and climate change.

Decadal changes in climate and ecosystems in the North Atlantic Ocean and adjacent seas

Climate change is unambiguous and its effects are clearly detected in all functional units of the Earth system. This study presents new analyses of sea-surface temperature changes and show that climate change is affecting ecosystems of the North Atlantic. Changes are seen from phytoplankton to zooplankton to fish and are modifying the dominance of species and the structure, the diversity and the functioning of marine ecosystems. Changes also range from phenological to biogeographical shifts and have involved in some regions of the Atlantic abrupt ecosystem shifts. These alterations reflect a response of pelagic ecosystems to a warmer temperature regime. Mechanisms are complex because they are nonlinear exhibiting tipping points and varying in space and time. Sensitivity of organisms to temperature changes is high, implicating that a small temperature modification can have sustained ecosystem effects. Implications of these changes for biogeochemical cycles are discussed. Two observed changes detected in the North Sea that could have opposite effects on carbon cycle are discussed. Increase in phytoplankton, as inferred from the phytoplankton colour index derived from the Continuous Plankton Recorder (CPR) survey, has been detected in the North Sea. This pattern has been accompanied by a reduction in the abundance of the herbivorous species Calanus finmarchicus. This might have reduced the grazing pressure and increase diatomaceous ‘fluff’, therefore carbon export in the North Sea. Therefore, it could be argued that the biological carbon pump might increase in this region with sea warming. In the meantime, however, the mean size of organisms (calanoid copepods) has dropped. Such changes have implications for the turnover time of biogenic carbon in plankton organisms and the mean residence time of particulate carbon they produce. The system characterising the warmer period is more based on recycling and less on export. The increase in the minimum turnover time indicates an increase in the ecosystem metabolism, which can be considered as a response of the pelagic ecosystems to climate warming. This phenomenon could reduce carbon export. These two opposite patterns of change are examples of the diversity of mechanisms and pathways the ecosystems may exhibit with climate change. Oversimplification of current biogeochemical models, often due to lack of data and biological understanding, could lead to wrong projection on the direction ecosystems and therefore some biogeochemical cycles might take in a warmer world.

Spatial variability of marine climate change impacts in the North Atlantic

There is an accumulating body of evidence to suggest that many marine ecosystems in the North Atlantic, both physically and biologically are responding to changes in regional climate caused predominately by the warming of air and sea surface temperatures (SST) and to a varying degree by the modification of oceanic currents, precipitation regimes and wind patterns. The biological manifestations of rising SST and oceanographic changes have variously taken the form of biogeographical, phenological, physiological and community changes. For example, during the last 40 years there has been a northerly movement of warmer water plankton by 10 degree latitude in the north-east Atlantic and a similar retreat of colder water plankton to the north. This geographical movement is much more pronounced than any documented terrestrial study, presumably due to advective processes playing an important role. Other research has shown that the plankton community in the North Sea has responded to changes in SST by adjusting their seasonality (in some cases a shift in seasonal cycles of over six weeks has been detected), but more importantly the response to climate warming varied between different functional groups and trophic levels, leading to mismatch. Therefore, while it has been documented that marine ecosystems in certain regions of the Atlantic have undergone some conspicuous changes over the last few decades it is not known whether this is a pan-oceanic homogenous response. Using these two most prominent responses and/or indicative signals of pelagic ecosystems to hydro-climatic change, changes in species phenology and the biogeographical movement of populations, we attempt to identify vulnerable regional areas in terms of particularly rapid and marked change.

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.

Long-term changes in the meroplankton of the North Sea

Data from the continuous plankton recorder (CPR) survey collected in the late-1940s to early-1960s indicated that the abundance of decapod larvae was low and the seasonal peak of abundance was late following cold winters. The phenological effect of temperature was shown to be consistent with relationships between both geographical and interannual patterns of variation. Analyses of CPR data collected from the 1940s to the present day reveal large-scale long-term changes in the abundance and phenology of the North Sea meroplankton. Echinoderm larvae, whose peak abundance has advanced by 47 days, show the greatest shift in timing. Echinoderm larvae have also increased in abundance to become the most abundant taxon in North Sea CPR samples. Genetic and morphological analyses of CPR samples show that the variations in echinoderm larvae are mainly attributable to an increasing abundance and earlier occurrence of the larvae of a resident species, Echinocardium cordatum, rather than a change in species composition. The remarkable scale of the changes in abundance and phenology of the meroplankton, which are greater than those seen in the holoplankton, has stimulated the development of further research into the causes and effects of these changes.

Phytoplankton phenology indices in coral reef ecosystems: Application to ocean-color observations in the Red Sea

Phytoplankton, at the base of the marine food web, represent a fundamental food source in coral reef ecosystems. The timing (phenology) and magnitude of the phytoplankton biomass are major determinants of trophic interactions. The Red Sea is one of the warmest and most saline basins in the world, characterized by an arid tropical climate regulated by the monsoon. These extreme conditions are particularly challenging for marine life. Phytoplankton phenological indices provide objective and quantitative metrics to characterize phytoplank- ton seasonality. The indices i.e. timings of initiation, peak, termination and duration are estimated here using 15 years (1997–2012) of remote sensing ocean-color data from the European Space Agency (ESA) Climate Change Initiative project (OC-CCI) in the entire Red Sea basin. The OC-CCI product, comprising merged and bias-corrected observations from three independent ocean-color sensors (SeaWiFS, MODIS and MERIS), and processed using the POLYMER algorithm (MERIS period), shows a significant increase in chlorophyll data cover- age, especially in the southern Red Sea during the months of summer NW monsoon. In open and reef-bound coastal waters, the performance of OC-CCI chlorophyll data is shown to be comparable with the performance of other standard chlorophyll products for the global oceans. These features have permitted us to investigate phytoplankton phenology in the entire Red Sea basin, and during both winter SE monsoon and summer NW monsoon periods. The phenological indices are estimated in the four open water provinces of the basin, and further examined at six coral reef complexes of particular socio-economic importance in the Red Sea, including Siyal Islands, Sharm El Sheikh, Al Wajh bank, Thuwal reefs, Al Lith reefs and Farasan Islands. Most of the open and deeper waters of the basin show an apparent higher chlorophyll concentration and longer duration of phyto- plankton growth during the winter period (relative to the summer phytoplankton growth period). In contrast, most of the reef-bound coastal waters display equal or higher peak chlorophyll concentrations and equal or lon- ger duration of phytoplankton growth during the summer period (relative to the winter phytoplankton growth period). The ecological and biological significance of the phytoplankton seasonal characteristics are discussed in context of ecosystem state assessment, and particularly to support further understanding of the structure and functioning of coral reef ecosystems in the Red Sea.