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.

From plankton to top predators: bottom-up control of a marine food web across four trophic levels

1. Abundant mid-trophic pelagic fish often play a central role in marine ecosystems, both as links between zooplankton and top predators and as important fishery targets. In the North Sea, the lesser sandeel occupies this position, being the main prey of many bird, mammal and fish predators and the target of a major industrial fishery. However, since 2003, sandeel landings have decreased by > 50%, and many sandeel-dependent seabirds experienced breeding failures in 2004. 2. Despite the major economic implications, current understanding of the regulation of key constituents of this ecosystem is poor. Sandeel abundance may be regulated 'bottom-up' by food abundance, often thought to be under climatic control, or 'top-down' by natural or fishery predation. We tested predictions from these two hypotheses by combining unique long-term data sets (1973–2003) on seabird breeding productivity from the Isle of May, SE Scotland, and plankton and fish larvae from the Continuous Plankton Recorder survey. We also tested whether seabird breeding productivity was more tightly linked to sandeel biomass or quality (size) of individual fish. 3. The biomass of larval sandeels increased two- to threefold over the study period and was positively associated with proxies of the abundance of their plankton prey. Breeding productivity of four seabirds bringing multiple prey items to their offspring was positively related to sandeel larval biomass with a 1-year lag, indicating dependence on 1-year-old fish, but in one species bringing individual fish it was strongly associated with the size of adult sandeels. 4. These links are consistent with bottom-up ecosystem regulation and, with evidence from previous studies, indicate how climate-driven changes in plankton communities can affect top predators and potentially human fisheries through the dynamics of key mid-trophic fish. However, the failing recruitment to adult sandeel stocks and the exceptionally low seabird breeding productivity in 2004 were not associated with low sandeel larval biomass in 2003, so other mechanisms (e.g. predation, lack of suitable food after metamorphosis) must have been important in this case. Understanding ecosystem regulation is extremely important for predicting the fate of keystone species, such as sandeels, and their predators.

Modelling the effects of climate change on the distribution and production of marine fishes: accounting for trophic interactions in a dynamic bioclimate envelope model

Climate change has already altered the distribution of marine fishes. Future predictions of fish distributions and catches based on bioclimate envelope models are available, but to date they have not considered interspecific interactions. We address this by combining the species-based Dynamic Bioclimate Envelope Model (DBEM) with a size-based trophic model. The new approach provides spatially and temporally resolved predictions of changes in species' size, abundance and catch potential that account for the effects of ecological interactions. Predicted latitudinal shifts are, on average, reduced by 20% when species interactions are incorporated, compared to DBEM predictions, with pelagic species showing the greatest reductions. Goodness-of-fit of biomass data from fish stock assessments in the North Atlantic between 1991 and 2003 is improved slightly by including species interactions. The differences between predictions from the two models may be relatively modest because, at the North Atlantic basin scale, (i) predators and competitors may respond to climate change together; (ii) existing parameterization of the DBEM might implicitly incorporate trophic interactions; and/or (iii) trophic interactions might not be the main driver of responses to climate. Future analyses using ecologically explicit models and data will improve understanding of the effects of inter-specific interactions on responses to climate change, and better inform managers about plausible ecological and fishery consequences of a changing environment.

An innovative statistical approach to constructing a readily comprehensible food web for a demersal fish community

Many food webs are so complex that it is difficult to distinguish the relationships between predators and their prey. We have therefore developed an approach that produces a food web which clearly demonstrates the strengths of the relationships between the predator guilds of demersal fish and their prey guilds in a coastal ecosystem. Subjecting volumetric dietary data for 35 abundant predators along the lower western Australia coast to cluster analysis and the SIMPROF routine separated the various species x length class combinations into 14 discrete predator guilds. Following nMDS ordination, the sequence of points for these predator guilds represented a 'trophic' hierarchy. This demonstrated that, with increasing body size, several species progressed upwards through this hierarchy, reflecting a marked change in diet, whereas others remained within the same guild. A novel use of cluster analysis and SIMPROF then identified each group of prey that was ingested in a common pattern across the full suite of predator guilds. This produced 12 discrete groups of taxa (prey guilds) that each typically comprised similar ecological/functional prey, which were then also aligned in a hierarchy. The hierarchical arrangements of the predator and prey guilds were plotted against each other to show the percentage contribution of each prey guild to the diet of each predator guild. The resultant shade plot demonstrates quantitatively how food resources are spread among the fish species and revealed that two prey guilds, one containing cephalopods and teleosts and the other small benthic/epibenthic crustaceans and polychaetes, were consumed by all predator guilds.

On the roles of cell size and trophic strategy in North Atlantic diatom and dinoflagellate communities

We have examined the inter- and intra-group seasonal succession of 113 diatom and dinoflagellate taxa, as surveyed by the Continuous Plankton Recorder (CPR) in the North Atlantic, by grouping taxa according to two key functional traits: cell size (mg C cell21) and trophic strategy (photoautotrophy, mixotrophy, or heterotrophy). Mixotrophic dinoflagellates follow photoautotrophic diatoms but precede their obligate heterotrophic counterparts in the succession because of the relative advantages afforded by photosynthesizing when light and nutrients are available in spring. The mean cell size of the sampled diatoms is smallest in the summer, likely because of the higher specific nutrient affinity of smaller relative to larger cells. Contrastingly, we hypothesize that mixotrophy diminishes the size selection based on nutrient limitation and accounts for the lack of a seasonal size shift among surveyed dinoflagellates. Relatively small, heterotrophic dinoflagellates (mg C cell21 , 1023) peak after other, larger dinoflagellates, in part because of the increased abundance of their small prey during nutrientdeplete summer months. The largest surveyed diatoms (mg C cell21 . 1022) bloom later than others, and we hypothesize that this may be because of their relatively slow maximum potential growth rates and high internal nutrient storage, as well as to the slower predation of these larger cells. The new trait database and analysis presented here helps translate the taxonomic information of the CPR survey into metrics that can be directly compared with trait-based models.

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.

The meso-scale response of subarctic North Pacific seabird community structure to lower trophic level abundance and diversity

Understanding the mechanisms that structure communities and influence biodiversity are fundamental goals of ecology. To test the hypothesis that the abundance and diversity of upper-trophic level predators (seabirds) is related to the underlying abundance and diversity of their prey (zooplankton) and ecosystem-wide energy availability (primary production), we initiated a monitoring program in 2002 that jointly and repeatedly surveys seabird and zooplankton populations across a 7,500 km British Columbia-Bering Sea-Japan transect. Seabird distributions were recorded by a single observer (MH) using a strip-width technique, mesozooplankton samples were collected with a Continuous Plankton Recorder, and primary production levels were derived using the appropriate satellite parameters and the Vertically Generalized Production Model (Behrenfeld and Falkowski 1997). Each trophic level showed clear spatio-temporal patterns over the course of the study. The strongest relationship between seabird abundance and diversity and the lower trophic levels was observed in March/April ('spring') and significant relationships were also found through June/July ('summer'). No discernable relationships were observed during the September/October ('fall') months. Overall, mesozooplankton abundance and biomass explained the dominant portion of seabird abundance and diversity indices (richness, Simpson's Index, and evenness), while primary production was only related to seabird richness. These findings underscore the notion that perturbations of ocean productivity and lower trophic level ecosystem constituents influenced by climate change, such as shifts in timing (phenology) and synchronicity (match-mismatch), could impart far-reaching consequences throughout the marine food web.

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.