Identifying predictable foraging habitats for a wide-ranging marine predator using ensemble ecological niche models

Aim: Ecological niche modelling can provide valuable insight into species' environmental preferences and aid the identification of key habitats for populations of conservation concern. Here, we integrate biologging, satellite remote-sensing and ensemble ecological niche models (EENMs) to identify predictable foraging habitats for a globally important population of the grey-headed albatross (GHA) Thalassarche chrysostoma. Location: Bird Island, South Georgia; Southern Atlantic Ocean. Methods: GPS and geolocation-immersion loggers were used to track at-sea movements and activity patterns of GHA over two breeding seasons (n = 55; brood-guard). Immersion frequency (landings per 10-min interval) was used to define foraging events. EENM combining Generalized Additive Models (GAM), MaxEnt, Random Forest (RF) and Boosted Regression Trees (BRT) identified the biophysical conditions characterizing the locations of foraging events, using time-matched oceanographic predictors (Sea Surface Temperature, SST; chlorophyll a, chl-a; thermal front frequency, TFreq; depth). Model performance was assessed through iterative cross-validation and extrapolative performance through cross-validation among years. Results: Predictable foraging habitats identified by EENM spanned neritic (<500 m), shelf break and oceanic waters, coinciding with a set of persistent biophysical conditions characterized by particular thermal ranges (3–8 °C, 12–13 °C), elevated primary productivity (chl-a > 0.5 mg m−3) and frequent manifestation of mesoscale thermal fronts. Our results confirm previous indications that GHA exploit enhanced foraging opportunities associated with frontal systems and objectively identify the APFZ as a region of high foraging habitat suitability. Moreover, at the spatial and temporal scales investigated here, the performance of multi-model ensembles was superior to that of single-algorithm models, and cross-validation among years indicated reasonable extrapolative performance. Main conclusions: EENM techniques are useful for integrating the predictions of several single-algorithm models, reducing potential bias and increasing confidence in predictions. Our analysis highlights the value of EENM for use with movement data in identifying at-sea habitats of wide-ranging marine predators, with clear implications for conservation and management.

Identifying predictable foraging habitats for a wide-ranging marine predator using ensemble ecological niche models

Aim: Ecological niche modelling can provide valuable insight into species' environmental preferences and aid the identification of key habitats for populations of conservation concern. Here, we integrate biologging, satellite remote-sensing and ensemble ecological niche models (EENMs) to identify predictable foraging habitats for a globally important population of the grey-headed albatross (GHA) Thalassarche chrysostoma. Location: Bird Island, South Georgia; Southern Atlantic Ocean. Methods: GPS and geolocation-immersion loggers were used to track at-sea movements and activity patterns of GHA over two breeding seasons (n = 55; brood-guard). Immersion frequency (landings per 10-min interval) was used to define foraging events. EENM combining Generalized Additive Models (GAM), MaxEnt, Random Forest (RF) and Boosted Regression Trees (BRT) identified the biophysical conditions characterizing the locations of foraging events, using time-matched oceanographic predictors (Sea Surface Temperature, SST; chlorophyll a, chl-a; thermal front frequency, TFreq; depth). Model performance was assessed through iterative cross-validation and extrapolative performance through cross-validation among years. Results: Predictable foraging habitats identified by EENM spanned neritic (<500 m), shelf break and oceanic waters, coinciding with a set of persistent biophysical conditions characterized by particular thermal ranges (3–8 °C, 12–13 °C), elevated primary productivity (chl-a > 0.5 mg m−3) and frequent manifestation of mesoscale thermal fronts. Our results confirm previous indications that GHA exploit enhanced foraging opportunities associated with frontal systems and objectively identify the APFZ as a region of high foraging habitat suitability. Moreover, at the spatial and temporal scales investigated here, the performance of multi-model ensembles was superior to that of single-algorithm models, and cross-validation among years indicated reasonable extrapolative performance. Main conclusions: EENM techniques are useful for integrating the predictions of several single-algorithm models, reducing potential bias and increasing confidence in predictions. Our analysis highlights the value of EENM for use with movement data in identifying at-sea habitats of wide-ranging marine predators, with clear implications for conservation and management.

Seasonal plankton dynamics along a cross-shelf gradient off northern Spain

The development of population models able to reproduce the dynamics of zooplankton is a central issue when trying to understand how a changing environment would affect zooplankton in the future. Using 10 years of monthly data on phytoplankton and zooplankton abundance in the Bay of Biscay from the IEO's RADIALES time-series programme, we built non-parametric Generalized Additive Models (GAMs) able to reproduce the dynamics of plankton on the basis of environmental factors (nutrients, temperature, upwelling and photoperiod). We found that the interaction between these two plankton components is approximately linear, whereas the effects of environmental factors are non-linear. With the inclusion of the environmental variability, the main seasonal and inter-annual dynamic patterns observed within the studied plankton assemblage indicate the prevalence of bottom-up regulatory control. The statistically deduced models were used to simulate the dynamics of the phytoplankton and zooplankton. A good agreement between observations and simulations was obtained, especially for zooplankton. We are presently developing spatio-temporal GAM models for the North Sea based on the Continuous Plankton Recorder database.

Quantifying the impact of environmental variables upon catch-per-unit-effort of the Blue Shark Prionace glauca in the Western English Channel

The effect of environmental variables on blue shark Prionace glauca catch per unit effort (CPUE) in a recreational fishery in the western English Channel, between June and September 1998–2011, was quantified using generalized additive models (GAMs). Sea surface temperature (SST) explained 1·4% of GAM deviance, and highest CPUE occurred at 16·7° C, reflecting the optimal thermal preferences of this species. Surface chlorophyll a concentration (CHL) significantly affected CPUE and caused 27·5% of GAM deviance. Additionally, increasing CHL led to rising CPUE, probably due to higher productivity supporting greater prey biomass. The density of shelf-sea tidal mixing fronts explained 5% of GAM deviance, but was non-significant, with increasing front density negatively affecting CPUE. Time-lagged frontal density significantly affected CPUE, however, causing 12·6% of the deviance in a second GAM and displayed a positive correlation. This outcome suggested a delay between the evolution of frontal features and the subsequent accumulation of productivity and attraction of higher trophic level predators, such as P. glauca.

Quantifying the impact of environmental variables upon catch-per-unit-effort of the Blue Shark Prionace glauca in the Western English Channel

The effect of environmental variables on blue shark Prionace glauca catch per unit effort (CPUE) in a recreational fishery in the western English Channel, between June and September 1998–2011, was quantified using generalized additive models (GAMs). Sea surface temperature (SST) explained 1·4% of GAM deviance, and highest CPUE occurred at 16·7° C, reflecting the optimal thermal preferences of this species. Surface chlorophyll a concentration (CHL) significantly affected CPUE and caused 27·5% of GAM deviance. Additionally, increasing CHL led to rising CPUE, probably due to higher productivity supporting greater prey biomass. The density of shelf-sea tidal mixing fronts explained 5% of GAM deviance, but was non-significant, with increasing front density negatively affecting CPUE. Time-lagged frontal density significantly affected CPUE, however, causing 12·6% of the deviance in a second GAM and displayed a positive correlation. This outcome suggested a delay between the evolution of frontal features and the subsequent accumulation of productivity and attraction of higher trophic level predators, such as P. glauca.

Mesoscale fronts as foraging habitats: composite front mapping reveals oceanographic drivers of habitat use for a pelagic seabird

The oceanographic drivers of marine vertebrate habitat use are poorly understood yet fundamental to our knowledge of marine ecosystem functioning. Here, we use composite front mapping and high-resolution GPS tracking to determine the significance of mesoscale oceanographic fronts as physical drivers of foraging habitat selection in northern gannets Morus bassanus. We tracked 66 breeding gannets from a Celtic Sea colony over 2 years and used residence time to identify area-restricted search (ARS) behaviour. Composite front maps identified thermal and chlorophyll-a mesoscale fronts at two different temporal scales—(i) contemporaneous fronts and (ii) seasonally persistent frontal zones. Using generalized additive models (GAMs), with generalized estimating equations (GEE-GAMs) to account for serial autocorrelation in tracking data, we found that gannets do not adjust their behaviour in response to contemporaneous fronts. However, ARS was more likely to occur within spatially predictable, seasonally persistent frontal zones (GAMs). Our results provide proof of concept that composite front mapping is a useful tool for studying the influence of oceanographic features on animal movements. Moreover, we highlight that frontal persistence is a crucial element of the formation of pelagic foraging hotspots for mobile marine vertebrates.

Modelling the future biogeography of North Atlantic zooplankton communities in response to climate change

Advances in habitat and climate modelling allow us to reduce uncertainties of climate change impacts on species distribution. We evaluated the impacts of future climate change on community structure, diversity, distribution and phenology of 14 copepod species in the North Atlantic. We developed and validated habitat models for key zooplankton species using continuous plankton recorder (CPR) survey data collected at mid latitudes of the North Atlantic. Generalized additive models (GAMs) were applied to relate the occurrence of species to environmental variables. Models were projected to future (2080–2099) environmental conditions using coupled hydroclimatix–biogeochemical models under the Intergovernmental Panel on Climate Change (IPCC) A1B climate scenario, and compared to present (2001–2020) conditions. Our projections indicated that the copepod community is expected to respond substantially to climate change: a mean poleward latitudinal shift of 8.7 km per decade for the overall community with an important species range variation (–15 to 18 km per decade); the species seasonal peak is expected to occur 12–13 d earlier for Calanus finmarchicus and C. hyperboreus; and important changes in community structure are also expected (high species turnover of 43–79% south of the Oceanic Polar Front). The impacts of the change expected by the end of the century under IPCC global warming scenarios on copepods highlight poleward shifts, earlier seasonal peak and changes in biodiversity spatial patterns that might lead to alterations of the future North Atlantic pelagic ecosystem. Our model and projections are supported by a temporal validation undertaken using the North Atlantic climate regime shift that occurred in the 1980s: the habitat model built in the cold period (1970–1986) has been validated in the warm period (1987–2004).

Future fish distributions constrained by depth in warming seas

European continental shelf seas have experienced intense warming over the past 30 years1. In the North Sea, fish have been comprehensively monitored throughout this period and resulting data provide a unique record of changes in distribution and abundance in response to climate change2, 3. We use these data to demonstrate the remarkable power of generalized additive models (GAMs), trained on data earlier in the time series, to reliably predict trends in distribution and abundance in later years. Then, challenging process-based models that predict substantial and ongoing poleward shifts of cold-water species4, 5, we find that GAMs coupled with climate projections predict future distributions of demersal (bottom-dwelling) fish species over the next 50 years will be strongly constrained by availability of habitat of suitable depth. This will lead to pronounced changes in community structure, species interactions and commercial fisheries, unless individual acclimation or population-level evolutionary adaptations enable fish to tolerate warmer conditions or move to previously uninhabitable locations.

Future fish distributions constrained by depth in warming seas

European continental shelf seas have experienced intense warming over the past 30 years1. In the North Sea, fish have been comprehensively monitored throughout this period and resulting data provide a unique record of changes in distribution and abundance in response to climate change2, 3. We use these data to demonstrate the remarkable power of generalized additive models (GAMs), trained on data earlier in the time series, to reliably predict trends in distribution and abundance in later years. Then, challenging process-based models that predict substantial and ongoing poleward shifts of cold-water species4, 5, we find that GAMs coupled with climate projections predict future distributions of demersal (bottom-dwelling) fish species over the next 50 years will be strongly constrained by availability of habitat of suitable depth. This will lead to pronounced changes in community structure, species interactions and commercial fisheries, unless individual acclimation or population-level evolutionary adaptations enable fish to tolerate warmer conditions or move to previously uninhabitable locations.

Drivers of euphausiid species abundance and numerical abundance in the Atlantic Ocean

Mid-ocean ridges are common features of the world’s oceans but there is a lack of understanding as to how their presence affects overlying pelagic biota. The Mid-Atlantic Ridge (MAR) is a dominant feature of the Atlantic Ocean. Here, we examined data on euphausiid distribution and abundance arising from several international research programmes and from the continuous plankton recorder. We used a generalized additive model (GAM) framework to explore spatial patterns of variability in euphausiid distribution on, and at either side of, the MAR from 60°N to 55°S in conjunction with variability in a suite of biological, physical and environmental parameters. Euphausiid species abundance peaked in mid-latitudes and was significantly higher on the ridge than in adjacent waters, but the ridge did not influence numerical abundance significantly. Sea surface temperature (SST) was the most important single factor influencing both euphausiid numerical abundance and species abundance. Increases in sea surface height variance, a proxy for mixing, increased the numerical abundance of euphausiids. GAM predictions of variability in species abundance as a function of SST and depth of the mixed layer were consistent with present theories, which suggest that pelagic niche availability is related to the thermal structure of the near surface water: more deeply-mixed water contained higher euphausiid biodiversity. In addition to exposing present distributional patterns, the GAM framework enables responses to potential future and past environmental variability including temperature change to be explored.

Effects of environmental conditions on the seasonal distribution of phytoplankton biomass in the North Sea

We study the spatial and seasonal variability of phytoplankton biomass (as phytoplankton color) in relation to the environmental conditions in the North Sea using data from the Continuous Plankton Recorder survey. By using only environmental fields and location as predictor variables we developed a nonparametric model (generalized additive model) to empirically explore how key environmental factors modulate the spatio-temporal patterns of the seasonal cycle of algal biomass as well as how these relate to the ,1988 North Sea regime shift. Solar radiation, as manifest through changes of sea surface temperature (SST), was a key factor not only in the seasonal cycle but also as a driver of the shift. The pronounced increase in SST and in wind speed after the 1980s resulted in an extension of the season favorable for phytoplankton growth. Nutrients appeared to be unimportant as explanatory variables for the observed spatio-temporal pattern, implying that they were not generally limiting factors. Under the new climatic regime the carrying capacity of the whole system has been increased and the southern North Sea, where the environmental changes have been more pronounced, reached a new maximum.

Variation among northeast Atlantic regions in the responses of zooplankton to climate change: Not all areas follow the same path

Broad scale climate forcing can interact with local environmental processes to affect the observed ecological phenomena. This causes potential problems of over-extrapolation for results from a limited number of sites or the averaging out of region-specific responses if data from too wide an area are combined. In this study, an area similar in extent to the Celtic Biscay Large Marine Ecosystem, but including off-shelf areas, was partitioned using clustering of satellite chlorophyll (chl-a) measurements. The resulting clusters were used to define areas over which to combine copepod data from the Continuous Plankton Recorder. Following filtering due to data limitations, nine regions were defined with sufficient records for analysis. These regions were consistent with known oceanographic structure in the study area. Off-shelf regions showed a progressively later timing in the seasonal peak of chl-a measurements moving northwards. Generalised additive models were used to estimate seasonal and multiannual signals in the adult and juvenile stages of Calanus finmarchicus, C. helgolandicus and the Paracalanus–Pseudocalanus group. Associations between variables (sea surface temperature (SST), phenology and annual abundance) differed among taxonomic groups, but even within taxonomic groups, relationships were not consistent across regions. For example, in the deep waters off Spain and Portugal the annual abundance of Calanus finmarchicus has a weak positive association with SST, in contrast to the pattern in most other regions. The regions defined in this study provide an objective basis for investigations into the long term dynamics of plankton populations and suggest suitable sub regions for deriving pelagic system indicators.

Basin-scale phenology and effects of climate variability on global timing of initial seaward migration of Atlantic salmon (Salmo salar)

Migrations between different habitats are key events in the lives of many organisms. Such movements involve annually recurring travel over long distances usually triggered by seasonal changes in the environment. Often, the migration is associated with travel to or from reproduction areas to regions of growth. Young anadromous Atlantic salmon (Salmo salar) emigrate from freshwater nursery areas during spring and early summer to feed and grow in the North Atlantic Ocean. The transition from the freshwater (parr') stage to the migratory stage where they descend streams and enter salt water (smolt') is characterized by morphological, physiological and behavioural changes where the timing of this parr-smolt transition is cued by photoperiod and water temperature. Environmental conditions in the freshwater habitat control the downstream migration and contribute to within- and among-river variation in migratory timing. Moreover, the timing of the freshwater emigration has likely evolved to meet environmental conditions in the ocean as these affect growth and survival of the post-smolts. Using generalized additive mixed-effects modelling, we analysed spatio-temporal variations in the dates of downstream smolt migration in 67 rivers throughout the North Atlantic during the last five decades and found that migrations were earlier in populations in the east than the west. After accounting for this spatial effect, the initiation of the downstream migration among rivers was positively associated with freshwater temperatures, up to about 10 degrees C and levelling off at higher values, and with sea-surface temperatures. Earlier migration occurred when river discharge levels were low but increasing. On average, the initiation of the smolt seaward migration has occurred 2.5days earlier per decade throughout the basin of the North Atlantic. This shift in phenology matches changes in air, river, and ocean temperatures, suggesting that Atlantic salmon emigration is responding to the current global climate changes.