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.

Diet of auklet chicks in the Aleutian Islands, Alaska: similarity among islands, interspecies overlap, and relationships to ocean climate

Seabirds are effective samplers of the marine environment, and can be used to measure resource partitioning among species and sites via food loads destined for chicks. We examined the composition, overlap, and relationships to changing climate and oceanography of 3,216 food loads from Least, Crested, and Whiskered Auklets (Aethia pusilla, A. cristatella, A. pygmaea) breeding in Alaska during 1994–2006. Meals comprised calanoid copepods (Neocalanus spp.) and euphausiids (Thysanoessa spp.) that reflect secondary marine productivity, with no difference among Buldir, Kiska, and Kasatochi islands across 585 km of the Aleutian Islands. Meals were very similar among species (mean Least–Crested Auklet overlap C = 0.68; Least–Whiskered Auklet overlap C = 0.96) and among sites, indicating limited partitioning of prey resources for auklets feeding chicks. The biomass of copepods and euphausiids in Least and Crested Auklet food loads was related negatively to the summer (June–July–August) North Pacific Gyre Oscillation, while in Whiskered Auklet food loads, this was negatively related to the winter (December–January–February) Pacific Decadal Oscillation, both of which track basin-wide sea-surface temperature (SST) anomalies. We found a significant quadratic relationship between the biomass of calanoid copepods in Least Auklet food loads at all three study sites and summer (June–July) SST, with maximal copepod biomass between 3–6°C (r 2 = 0.71). Outside this temperature range, zooplankton becomes less available to auklets through delayed development. Overall, our results suggest that auklets are able to buffer climate-mediated bottom-up forcing of demographic parameters like productivity, as the composition of chick meals has remained constant over the course of our study.

Warm-water decapods and the trophic amplification of climate in the North Sea

A long-term time series of plankton and benthic records in the North Sea indicates an increase in decapods and a decline in their prey species that include bivalves and flatfish recruits. Here, we show that in the southern North Sea the proportion of decapods to bivalves doubled following a temperature-driven, abrupt ecosystem shift during the 1980s. Analysis of decapod larvae in the plankton reveals a greater presence and spatial extent of warm-water species where the increase in decapods is greatest. These changes paralleled the arrival of new species such as the warm-water swimming crab Polybius henslowii now found in the southern North Sea. We suggest that climate-induced changes among North Sea decapods have played an important role in the trophic amplification of a climate signal and in the development of the new North Sea dynamic regime.

Spatial variability of the plankton trophic interaction in the North Sea: a new feature after the early 1970s

Traditionally, marine ecosystem structure was thought to be bottom-up controlled. In recent years, a number of studies have highlighted the importance of top-down regulation. Evidence is accumulating that the type of trophic forcing varies temporally and spatially, and an integrated view – considering the interplay of both types of control – is emerging. Correlations between time series spanning several decades of the abundances of adjacent trophic levels are conventionally used to assess the type of control: bottom-up if positive or top-down if this is negative. This approach implies averaging periods which might show time-varying dynamics and therefore can hide part of this temporal variability. Using spatially referenced plankton information extracted from the Continuous Plankton Recorder, this study addresses the potential dynamic character of the trophic structure at the planktonic level in the North Sea by assessing its variation over both temporal and spatial scales. Our results show that until the early-1970s a bottom-up control characterized the base of the food web across the whole North Sea, with diatoms having a positive and homogeneous effect on zooplankton filter-feeders. Afterwards, different regional trophic dynamics were observed, in particular a negative relationship between total phytoplankton and zooplankton was detected off the west coast of Norway and the Skagerrak as opposed to a positive one in the southern reaches. Our results suggest that after the early 1970s diatoms remained the main food source for zooplankton filter-feeders east of Orkney–Shetland and off Scotland, while in the east, from the Norwegian Trench to the German Bight, filter-feeders were mainly sustained by dinoflagellates.

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.

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.

Investigating the inter-relationships between water attenuated irradiance, primary production and DMS(P)

Both solar irradiance and primary production have been proposed as independent controls on seawater dimethyl sulphide (DMS) and dimethylsulphoniopropionate (DMSP) concentrations. However, irradiance also drives photosynthesis, and thus influences a complex set of inter-related processes that modulate marine DMS. We investigate the potential inter-relationships between the rate of primary production (carbon assimilation), water-attenuated irradiance and DMS/DMSP dynamics by applying correlation analysis to a high resolution, concurrently sampled in situ data set from a range of latitudes covering multiple biogeochemical provinces from 3 of the 4 Longhurst biogeochemical domains. The combination of primary production (PP) and underwater irradiance (Iz) within a multivariate regression model is able to explain 55% of the variance in DMS concentrations from all depths within the euphotic zone and 66% of the variance in surface DMS concentrations. Contrary to some previous studies we find a variable representing biological processes is necessary to better account for the variance in DMS. We find that the inclusion of Iz accounts for variance in DMS that is independent from the variance explained by PP. This suggests an important role for solar irradiance (beyond the influence of irradiance upon primary production) in mediating the relationship between the productivity of the ecosystem, DMS/DMSP production and ambient seawater DMS concentrations.

Quantifying ecosystem-level consequences of ocean acidification and warming by scaling up individual level responses of a predator snail and its trophic interactions

Understanding long‐term, ecosystem‐level impacts of climate change is challenging because experimental research frequently focuses on short‐term, individual‐level impacts in isolation. We address this shortcoming first through an interdisciplinary ensemble of novel experimental techniques to investigate the impacts of 14‐month exposure to ocean acidification and warming (OAW) on the physiology, activity, predatory behaviour and susceptibility to predation of an important marine gastropod (Nucella lapillus). We simultaneously estimated the potential impacts of these global drivers on N. lapillus population dynamics and dispersal parameters. We then used these data to parameterize a dynamic bioclimatic envelope model, to investigate the consequences of OAW on the distribution of the species in the wider NE Atlantic region by 2100. The model accounts also for changes in the distribution of resources, suitable habitat and environment simulated by finely resolved biogeochemical models, under three IPCC global emissions scenarios. The experiments showed that temperature had the greatest impact on individual‐level responses, while acidification had a similarly important role in the mediation of predatory behaviour and susceptibility to predators. Changes in Nucella predatory behaviour appeared to serve as a strategy to mitigate individual‐level impacts of acidification, but the development of this response may be limited in the presence of predators. The model projected significant large‐scale changes in the distribution of Nucella by the year 2100 that were exacerbated by rising greenhouse gas emissions. These changes were spatially heterogeneous, as the degree of impact of OAW on the combination of responses considered by the model varied depending on local‐environmental conditions and resource availability. Such changes in macro‐scale distributions cannot be predicted by investigating individual‐level impacts in isolation, or by considering climate stressors separately. Scaling up the results of experimental climate change research requires approaches that account for long‐term, multiscale responses to multiple stressors, in an ecosystem context.

Assessing the potential of autonomous submarine gliders for ecosystem monitoring across multiple trophic levels (plankton to cetaceans) in shallow shelf seas

A combination of scientific, economic, technological and policy drivers is behind a recent upsurge in the use of marine autonomous systems (and accompanying miniaturized sensors) for environmental mapping and monitoring. Increased spatial–temporal resolution and coverage of data, at reduced cost, is particularly vital for effective spatial management of highly dynamic and heterogeneous shelf environments. This proof-of-concept study involves integration of a novel combination of sensors onto buoyancy-driven submarine gliders, in order to assess their suitability for ecosystem monitoring in shelf waters at a variety of trophic levels. Two shallow-water Slocum gliders were equipped with CTD and fluorometer to measure physical properties and chlorophyll, respectively. One glider was also equipped with a single-frequency echosounder to collect information on zooplankton and fish distribution. The other glider carried a Passive Acoustic Monitoring system to detect and record cetacean vocalizations, and a passive sampler to detect chemical contaminants in the water column. The two gliders were deployed together off southwest UK in autumn 2013, and targeted a known tidal-mixing front west of the Isles of Scilly. The gliders’ mission took about 40 days, with each glider travelling distances of >1000 km and undertaking >2500 dives to depths of up to 100 m. Controlling glider flight and alignment of the two glider trajectories proved to be particularly challenging due to strong tidal flows. However, the gliders continued to collect data in poor weather when an accompanying research vessel was unable to operate. In addition, all glider sensors generated useful data, with particularly interesting initial results relating to subsurface chlorophyll maxima and numerous fish/cetacean detections within the water column. The broader implications of this study for marine ecosystem monitoring with submarine gliders are discussed.

Macrofauna along the Sudanese Red Sea coast: potential effect of mangrove clearance on community and trophic structure

Mangroves along the Sudanese Red Sea coast are under constant anthropogenic pressure. To better understand the influence of mangrove clearance on the intertidal benthic community, we investigated the composition, biodiversity and standing stock of the macrofauna communities at high-, mid- and low-water levels in three contrasting habitats: a bare sand flat, a cleared mangrove and an intact mangrove. In addition, a community-wide metric approach based on taxon-specific carbon and nitrogen isotope values was used to compare the trophic structure between the three habitats. The habitats differed significantly in terms of macrofaunal standing stock, community composition and trophic structure. The high- and mid-water levels of the intact mangroves showed a distinct macrofaunal community characterized by elevated densities and biomass, largely governed by higher decapod and gastropod abundances. Diversity was similar for cleared and intact mangroves, but much lower for the bare sand flat. Community-wide metrics indicated highest trophic diversity and community niche breadth in the intact mangroves. Differences between the cleared and intact mangroves can be partly attributed to differences in sediment characteristics resulting from mangrove clearance. These results suggest a significant impact of mangrove clearance on the macrofaunal community and trophic structure. This study calls for further investigations and management actions to protect and restore these habitats, and ensure the survival of this ecologically valuable coastal ecosystem.

Assessing the potential of autonomous submarine gliders for ecosystem monitoring across multiple trophic levels (plankton to cetaceans) in shallow shelf seas

A combination of scientific, economic, technological and policy drivers is behind a recent upsurge in the use of marine autonomous systems (and accompanying miniaturized sensors) for environmental mapping and monitoring. Increased spatial–temporal resolution and coverage of data, at reduced cost, is particularly vital for effective spatial management of highly dynamic and heterogeneous shelf environments. This proof-of-concept study involves integration of a novel combination of sensors onto buoyancy-driven submarine gliders, in order to assess their suitability for ecosystem monitoring in shelf waters at a variety of trophic levels. Two shallow-water Slocum gliders were equipped with CTD and fluorometer to measure physical properties and chlorophyll, respectively. One glider was also equipped with a single-frequency echosounder to collect information on zooplankton and fish distribution. The other glider carried a Passive Acoustic Monitoring system to detect and record cetacean vocalizations, and a passive sampler to detect chemical contaminants in the water column. The two gliders were deployed together off southwest UK in autumn 2013, and targeted a known tidal-mixing front west of the Isles of Scilly. The gliders’ mission took about 40 days, with each glider travelling distances of >1000 km and undertaking >2500 dives to depths of up to 100 m. Controlling glider flight and alignment of the two glider trajectories proved to be particularly challenging due to strong tidal flows. However, the gliders continued to collect data in poor weather when an accompanying research vessel was unable to operate. In addition, all glider sensors generated useful data, with particularly interesting initial results relating to subsurface chlorophyll maxima and numerous fish/cetacean detections within the water column. The broader implications of this study for marine ecosystem monitoring with submarine gliders are discussed.

Questioning the role of phenology shifts and trophic mismatching in a planktonic food web

In a warming climate, differential shifts in the seasonal timing of predators and prey have been suggested to lead to trophic ‘‘mismatches’’ that decouple primary, secondary and tertiary production. We tested this hypothesis using a 25-year time-series of weekly sampling at the Plymouth L4 site, comparing 57 plankton taxa spanning 4 trophic levels. During warm years, there was a weak tendency for earlier timings of spring taxa and later timings of autumn taxa. While this is in line with many previous findings, numerous exceptions existed and only a few taxa (e.g. Gyrodinium spp., Pseudocalanus elongatus, and Acartia clausi) showed consistent, strong evidence for temperature-related timing shifts, revealed by all 4 of the timing indices that we used. Also, the calculated offsets in timing i.e. ‘‘mismatches’’) between predator and prey were no greater in extreme warm or cold years than during more average years. Further, the magnitude of these offsets had no effect on the ‘‘success’’ of the predator, in terms of their annual mean abundance or egg production rates. Instead numerous other factors override, including: inter-annual variability in food quantity, high food baseline levels, turnover rates and prolonged seasonal availability, allowing extended periods of production. Furthermore many taxa, notably meroplankton, increased well before the spring bloom. While theoretically a chronic mismatch, this likely reflects trade-offs for example in predation avoidance. Various gelatinous taxa (Phaeocystis, Noctiluca, ctenophores, appendicularians, medusae) may have reduced these predation constraints, with variable, explosive population outbursts likely responding to improved conditions. The match–mismatch hypothesis may apply for highly seasonal, pulsed systems or specialist feeders, but we suggest that the concept is being over-extended to other marine systems where multiple factors compensate.

ERSEM 15.06: a generic model for marine biogeochemistry and the ecosystem dynamics of the lower trophic levels

The ERSEM model is one of the most established ecosystem models for the lower trophic levels of the marine food-web in the scientific literature. Since its original development in the early nineties it has evolved significantly from a coastal ecosystem model for the North-Sea to a generic tool for ecosystem simulations from shelf seas to the global ocean. The current model release contains all essential elements for the pelagic and benthic part of the marine ecosystem, including the microbial food-web, the carbonate system and calcification. Its distribution is accompanied by a testing framework enabling the analysis of individual parts of the model. Here we provide a detailed mathematical description of all ERSEM components along with case-studies of mesocosm type simulations, water column implementations and a brief example of a full-scale application for the North-West European shelf. Validation against in situ data demonstrates the capability of the model to represent the marine ecosystem in contrasting environments.