Climatic effects on the phenology of lake processes

Populations living in seasonal environments are exposed to systematic changes in physical conditions that restrict the growth and reproduction of many species to only a short time window of the annual cycle. Several studies have shown that climate changes over the latter part of the 20th century affected the phenology and population dynamics of single species. However, the key limitation to forecasting the effects of changing climate on ecosystems lies in understanding how it will affect interactions among species. We investigated the effects of climatic and biotic drivers on physical and biological lake processes, using a historical dataset of 40 years from Lake Washington, USA, and dynamic time‐series models to explain changes in the phenological patterns among physical and biological components of pelagic ecosystems. Long‐term climate warming and variability because of large‐scale climatic patterns like Pacific decadal oscillation (PDO) and El Niño–southern oscillation (ENSO) extended the duration of the stratification period by 25 days over the last 40 years. This change was due mainly to earlier spring stratification (16 days) and less to later stratification termination in fall (9 days). The phytoplankton spring bloom advanced roughly in parallel to stratification onset and in 2002 it occurred about 19 days earlier than it did in 1962, indicating the tight connection of spring phytoplankton growth to turbulent conditions. In contrast, the timing of the clear‐water phase showed high variability and was mainly driven by biotic factors. Among the zooplankton species, the timing of spring peaks in the rotifer Keratella advanced strongly, whereas Leptodiaptomus and Daphnia showed slight or no changes. These changes have generated a growing time lag between the spring phytoplankton peak and zooplankton peak, which can be especially critical for the cladoceran Daphnia. Water temperature, PDO, and food availability affected the timing of the spring peak in zooplankton. Overall, the impact of PDO on the phenological processes were stronger compared with ENSO. Our results highlight that climate affects physical and biological processes differently, which can interrupt energy flow among trophic levels, making ecosystem responses to climate change difficult to forecast.     

Copepod life cycle adaptations and success in response to phytoplankton spring bloom phenology

In a seasonal environment, the timing of reproduction is usually scheduled to maximize the survival of offspring. Within deep water bodies, the phytoplankton spring bloom provides a short time window of high food quantity and quality for herbivores. The onset of algal bloom development, however, varies strongly from year to year due to interannual variability in meteorological conditions. Furthermore, the onset is predicted to change with global warming. Here, we use a long-term dataset to study (a) how a cyclopoid copepod, Cyclops vicinus , is dealing with the large variability in phytoplankton bloom phenology, and (b) if bloom phenology has an influence on offspring numbers. C. vicinus performed a two-phase dormancy, that is, the actual diapause of fourth copepodid stages at the lake bottom is followed by a delay in maturation, that is, a quiescence, within the fifth copepodid stage until the start of the spring bloom. This strategy seems to guarantee a high temporal match of the food requirements for successful offspring development, especially through the highly vulnerable naupliar stages, with the phytoplankton spring bloom. However, despite this match with food availability in all study years, offspring numbers, that is, offspring survival rates were higher in years with an early start of the phytoplankton bloom. In addition, the phenology of copepod development suggested that also within study years, early offspring seems to have lower mortality rates than late produced offspring. We suggest that this is due to a longer predator-free time period and/or reduced time stress for development. Hence, within the present climate variability, the copepod benefited from warmer spring temperatures resulting in an earlier phytoplankton spring bloom. Time will show if the copepod's strategy is flexible enough to cope with future warming.     

Earlier onset of the spring phytoplankton bloom in lakes of the temperate zone in a warmer climate

The decoupling of trophic interactions is potentially one of the most severe consequences of climate warming. In lakes and oceans the timing of phytoplankton blooms affects competition within the plankton community as well as food–web interactions with zooplankton and fish. Using Upper Lake Constance as an example, we present a model‐based analysis that predicts that in a future warmer climate, the onset of the spring phytoplankton bloom will occur earlier in the year than it does at present. This is a result of the earlier occurrence of the transition from strong to weak vertical mixing in spring, and of the associated earlier onset of stratification. According to our simulations a shift in the timing of phytoplankton growth resulting from a consistently warmer climate will exceed that resulting from a single unusually warm year. The numerical simulations are complemented by a statistical analysis of long‐term data from Upper Lake Constance which demonstrates that oligotrophication has a negligible effect on the timing of phytoplankton growth in spring and that an early onset of the spring phytoplankton bloom is associated with high air temperatures and low wind speeds.     

Detection of climate change‐driven trends in phytoplankton phenology

The timing of the annual phytoplankton spring bloom is likely to be altered in response to climate change. Quantifying that response has, however, been limited by the typically coarse temporal resolution (monthly) of global climate models. Here, we use higher resolution model output (maximum 5 days) to investigate how phytoplankton bloom timing changes in response to projected 21st century climate change, and how the temporal resolution of data influences the detection of long‐term trends. We find that bloom timing generally shifts later at mid‐latitudes and earlier at high and low latitudes by ~5 days per decade to 2100. The spatial patterns of bloom timing are similar in both low (monthly) and high (5 day) resolution data, although initiation dates are later at low resolution. The magnitude of the trends in bloom timing from 2006 to 2100 is very similar at high and low resolution, with the result that the number of years of data needed to detect a trend in phytoplankton phenology is relatively insensitive to data temporal resolution. We also investigate the influence of spatial scales on bloom timing and find that trends are generally more rapidly detectable after spatial averaging of data. Our results suggest that, if pinpointing the start date of the spring bloom is the priority, the highest possible temporal resolution data should be used. However, if the priority is detecting long‐term trends in bloom timing, data at a temporal resolution of 20 days are likely to be sufficient. Furthermore, our results suggest that data sources which allow for spatial averaging will promote more rapid trend detection.     

Seasonality of North Atlantic phytoplankton from space: impact of environmental forcing on a changing phenology (1998–2012)

Seasonal pulses of phytoplankton drive seasonal cycles of carbon fixation and particle sedimentation, and might condition recruitment success in many exploited species. Taking advantage of long‐term series of remotely sensed chlorophyll a (1998–2012), we analyzed changes in phytoplankton seasonality in the North Atlantic Ocean. Phytoplankton phenology was analyzed based on a probabilistic characterization of bloom incidence. This approach allowed us to detect changes in the prevalence of different seasonal cycles and, at the same time, to estimate bloom timing and magnitude taking into account uncertainty in bloom detection. Deviations between different sensors stressed the importance of a prolonged overlap between successive missions to ensure a correct assessment of phenological changes, as well as the advantage of semi‐analytical chlorophyll algorithms over empirical ones to reduce biases. Earlier and more intense blooms were detected in the subpolar Atlantic, while advanced blooms of less magnitude were common in the Subtropical gyre. In the temperate North Atlantic, spring blooms advanced their timing and decreased in magnitude, whereas fall blooms delayed and increased their intensity. At the same time, the prevalence of locations with a single autumn/winter bloom or with a bimodal seasonal cycle increased, in consonance with a poleward expansion of subtropical conditions. Changes in bloom timing and magnitude presented a clear signature of environmental factors, especially wind forcing, although changes on incident photosynthetically active radiation and sea surface temperature were also important depending on latitude. Trends in bloom magnitude matched changes in mean chlorophyll a during the study period, suggesting that seasonal peaks drive long‐term trends in chlorophyll a concentration. Our results link changes in North Atlantic climate with recent trends in the phenology of phytoplankton, suggesting an intensification of these impacts in the near future.     

Water temperature and stratification depth independently shift cardinal events during plankton spring succession

In deep temperate lakes, the beginning of the growing season is triggered by thermal stratification, which alleviates light limitation of planktonic producers in the surface layer and prevents heat loss to deeper strata. The sequence of subsequent phenological events (phytoplankton spring bloom, grazer peak, clearwater phase) results in part from coupled phytoplankton–grazer interactions. Disentangling the separate, direct effects of correlated climatic drivers (stratification‐dependent underwater light climate vs. water temperature) from their indirect effects mediated through trophic feedbacks is impossible using observational field data, which challenges our understanding of global warming effects on seasonal plankton dynamics. We therefore manipulated water temperature and stratification depth independently in experimental field mesocosms containing ambient microplankton and inocula of the resident grazer Daphnia hyalina. Higher light availability in shallower surface layers accelerated primary production, warming accelerated consumption and growth of Daphnia, and both factors speeded up successional dynamics driven by trophic feedbacks. Specifically, phytoplankton peaked and decreased earlier and Daphnia populations increased and peaked earlier at both shallower stratification and higher temperature. The timing of ciliate dynamics was unrelated to both factors. Volumetric peak densities of phytoplankton, ciliates and Daphnia in the surface layer were also unaffected by temperature but declined with stratification depth in parallel with light availability. The latter relationship vanished, however, when population sizes were integrated over the entire water column. Overall our results suggest that, integrated over the entire water column of a deep lake, surface warming and shallower stratification independently speed up spring successional events, whereas the magnitudes of phytoplankton and zooplankton spring peaks are less sensitive to these factors. Therefore, accelerated dynamics under warming need not lead to a trophic mismatch (given similar grazer inocula at the time of stratification). We emphasize that entire water column dynamics must be studied to estimate global warming effects on lake ecosystems.     

Temporal trends in phenology of the honey bee Apis mellifera (L.) and the small white Pieris rapae (L.) in the Iberian Peninsula (1952–2004)

Abstract.  1. The first adult appearance of two insect species, the honey bee Apis mellifera (L.) and the small white Pieris rapae (L.), was examined between 1952 and 2004 in Spain.
2. After factoring out the variability resulting from the broad geographical and topographical range of the 798 sampling localities, multiple regression models were used to detect temporal trends in phenology.
3. The best models were repeated, including spring temperature as the explanatory variable to examine the effects of climate on appearance phenology.
4. Both species showed similar temporal trends, delaying their appearance phenology until the mid-1970s and advancing it since that time.
5. The appearance times for both species were negatively related to mean temperature between February and April, with both species appearing earlier in years with warmer springs.
6. The strong dependence of appearance dates on temperature indicates that climatic fluctuations are primarily responsible for the inter-annual variability in spring appearance phenology of both species, and consequently account for the observed long-term trends.
7. This study demonstrates that insect phenology is an accurate and sensitive bioindicator of climate change.     

Centennial decline in North Sea water clarity causes strong delay in phytoplankton bloom timing

With climate warming, a widespread expectation is that events in spring, such as flowering, bird migrations, and insect bursts, will occur earlier because of increasing temperature. At high latitudes, increased ocean temperature is suggested to advance the spring phytoplankton bloom due to earlier stabilization of the water column. However, climate warming is also expected to cause browning in lakes and rivers due to increases in terrestrial greening, ultimately reducing water clarity in coastal areas where freshwater drain. In shallow areas, decreased retention of sediments on the seabed will add to this effect. Both browning and resuspension of sediments imply a reduction of the euphotic zone and Sverdrup's critical depth leading to a delay in the spring bloom, counteracting the effect of increasing temperature. Here, we provide evidence that such a transparency reduction has already taken place in both the deep and shallow areas of the North Sea during the 20th century. A sensitivity analysis using a water column model suggests that the reduced transparency might have caused up to 3 weeks delay in the spring bloom over the last century. This delay stands in contrast to the earlier bloom onset expected from global warming, thus highlighting the importance of including changing water transparency in analyses of phytoplankton phenology and primary production. This appears to be of particular relevance for coastal waters, where increased concentrations of absorbing and scattering substances (sediments, dissolved organic matter) have been suggested to lead to coastal darkening.     

Testing the Sensitivity of Phytoplankton Communities to Changes in Water Temperature and Nutrient Load, in a Temperate Lake

Freshwater lakes are biologically sensitive to changes in the surrounding environment and the impacts that such changes have on their water quality are of considerable ecological, recreational and economic importance. In this study the phytoplankton community model, PROTECH, was used to experiment with the effects of elevated temperatures and increased nutrient load on phytoplankton succession and productivity. The response of a phytoplankton community to combined incremental changes in these drivers was analysed, in order to elucidate the resulting ecological changes. Annual mean phytoplankton biomass increased with increases in temperature and nutrient loading, although the latter had the larger effect. The phenology of the dominant phytoplankton taxa changed with increasing water temperature; the three spring blooming species all peaked earlier in the year. The simulated summer bloom of Anabaena became earlier in the year and the Chlorella bloom later. The increased phytoplankton biomass was largely dominated by the cyanobacterium Anabaena, which was especially prevalent during the summer bloom. This resulted in a progressive loss of phytoplankton biodiversity with increasing water temperature and nutrient supply. Model experimentation showed that whilst both factors greatly affected the community, the changes to nutrient loading generally had the greater effect and that at low nutrient levels the effect of water temperature change was reduced considerably. Finally, the model predicted that cyanobacteria have the potential to dominate the phytoplankton community, with clear consequences for water quality, and that this dominance was at its greatest when high water temperatures were combined with high nutrient loads.     

Climate change impacts on mismatches between phytoplankton blooms and fish spawning phenology

Substantial interannual variability in marine fish recruitment (i.e., the number of young fish entering a fishery each year) has been hypothesized to be related to whether the timing of fish spawning matches that of seasonal plankton blooms. Environmental processes that control the phenology of blooms, such as stratification, may differ from those that influence fish spawning, such as temperature‐linked reproductive maturation. These different controlling mechanisms could cause the timing of these events to diverge under climate change with negative consequences for fisheries. We use an earth system model to examine the impact of a high‐emissions, climate‐warming scenario (RCP8.5) on the future spawning time of two classes of temperate, epipelagic fishes: “geographic spawners” whose spawning grounds are defined by fixed geographic features (e.g., rivers, estuaries, reefs) and “environmental spawners” whose spawning grounds move responding to variations in environmental properties, such as temperature. By the century's end, our results indicate that projections of increased stratification cause spring and summer phytoplankton blooms to start 16 days earlier on average (±0.05 days SE) at latitudes >40°N. The temperature‐linked phenology of geographic spawners changes at a rate twice as fast as phytoplankton, causing these fishes to spawn before the bloom starts across >85% of this region. “Extreme events,” defined here as seasonal mismatches >30 days that could lead to fish recruitment failure, increase 10‐fold for geographic spawners in many areas under the RCP8.5 scenario. Mismatches between environmental spawners and phytoplankton were smaller and less widespread, although sizable mismatches still emerged in some regions. This indicates that range shifts undertaken by environmental spawners may increase the resiliency of fishes to climate change impacts associated with phenological mismatches, potentially buffering against declines in larval fish survival, recruitment, and fisheries. Our model results are supported by empirical evidence from ecosystems with multidecadal observations of both fish and phytoplankton phenology.     

Changing temperature regimes have advanced the phenology of Odonata in the Netherlands

Abstract.  1. Responses of biota to climate change have been well documented for a restricted number of taxa. This study examined shifts in phenology of 37 species of the aquatic insect order Odonata in the Netherlands over the last decade.
2. The present study shows that adults of the Dutch dragonflies and damselflies have advanced their flight dates over recent years due to complex effects of changing temperature regimes on the timing of adult flight dates.
3. Flight dates did not respond to changes in autumn/winter temperatures, advanced with increases in spring temperatures of the focal and previous year, and delayed with increases in summer temperatures of the previous year. Climate change consequently advanced the flight dates of the Odonata because only spring temperatures have increased during the study period.
4. The findings imply that climate change can evoke strong phenological responses in aquatic insects. Moreover, shifts in phenology due to climate change are likely to vary both spatially or temporally, depending on the exact nature of climate change.     

Increased sea ice melt as a driver of enhanced Arctic phytoplankton blooming

Phytoplankton primary production in the Arctic Ocean has been increasing over the last two decades. In 2019, a record spring bloom occurred in Fram Strait, characterized by a peak in chlorophyll that was reached weeks earlier than in other years and was larger than any previously recorded May bloom. Here, we consider the conditions that led to this event and examine drivers of spring phytoplankton blooms in Fram Strait using in situ, remote sensing, and data assimilation methods. From samples collected during the May 2019 bloom, we observe a direct relationship between sea ice meltwater in the upper water column and chlorophyll a pigment concentrations. We place the 2019 spring dynamics in context of the past 20 years, a period marked by rapid change in climatic conditions. Our findings suggest that increased advection of sea ice into the region and warmer surface temperatures led to a rise in meltwater input and stronger near-surface stratification. Over this time period, we identify large-scale spatial correlations in Fram Strait between increased chlorophyll a concentrations and increased freshwater flux from sea ice melt.     

Migration of anadromous brown trout Salmo trutta in a Norwegian river

1. Upstream and downstream migrating anadromous brown trout Salmo trutta were monitored daily in fish traps in the River Imsa in south-western Norway for 24 years, from 1976 to 1999. One-third of the fish descended to sea during spring (February–June) and two-thirds during autumn (September–January).
2. In spring, high water temperature appeared to influence the downstream descent. Large brown trout (> 30 cm, chiefly two or more sea sojourns) descended earlier and appeared less dependent on high water temperature than smaller and younger fish. The spring water flow was generally low and of little importance for the descent.
3. In autumn, the daily number of descending brown trout correlated positively with flow and negatively with water temperature.
4. Brown trout ascended from the sea between April and December, but more than 70% ascended between August and October. The number of ascending trout increased significantly with both decreasing temperature and flow during the autumn. This response to flow appeared to be the result of the autumn discharge which is generally high and most fish ascended at an intermediate flow of 7.5–10 m³ s⁻¹ (which is low for the season).
5. In a river like the Imsa with low spring and high autumn flows, water temperature appears to be the main environmental factor influencing the timing and rate of spring descent, while both water temperature and flow seemed to influence the timing and rate of the autumn descent and ascent. These relationships make sea trout migrations susceptible to variation in climate and human impacts of the flow regime in rivers.     

Are phytoplankton blooms occurring earlier in the Arctic?

Time series of satellite‐derived surface chlorophyll‐a concentration (Chl) in 1997–2009 were used to examine for trends in the timing of the annual phytoplankton bloom maximum. Significant trends towards earlier phytoplankton blooms were detected in about 11% of the area of the Arctic Ocean with valid Chl data, e.g. in the Hudson Bay, Foxe Basin, Baffin Sea, off the coasts of Greenland, in the Kara Sea and around Novaya Zemlya. These areas roughly coincide with areas where ice concentration has decreased in early summer (June), thus making the earlier blooms possible. In the selected areas, the annual phytoplankton bloom maximum has advanced by up to 50 days which may have consequences for the Arctic food chain and carbon cycling. Outside the Arctic, the annual Chl maximum has become earlier in boreal North Pacific but later in the North Atlantic.     

A modelling investigation of the distribution of stratification and phytoplankton abundance in the Irish Sea

Thermal stratification and phytoplankton abundance are modelledon a 5 km grid covering the Irish Sea. The water column is approximatedby three layers. The top layer is uniformly mixed by wind stirringand the bottom by tidal energy, while linear gradients can occurin the middle layer. The model is forced with hourly meteorologicaldata and mean tidal energies. Primary production is representedby a model with a single nutrient and a single phytoplanktonpopulation. The results from the model show good agreement withdata collected on a Ministry of Agriculture, Fisheries and Food(MAFF) cruise in May 1992 and with historical data. When advectionis included, driven by depth-averaged currents, the surfacetemperature patterns are improved but bottom temperatures indeep water are raised and high concentrations of chlorophyllare carried offshore from coastal regions. This indicates alimitation of using depth-averaged currents and a need to accountfor differences in phytoplankton species composition in coastaland offshore waters. Calculations demonstrate the importanceof salinity variations to stratification and phytoplankton growth.Smoothing the wind mixing energy has the effect of delayingthe onset of the spring bloom in areas where wind mixing issignificant. Removing the diurnal cycle of solar heating alsodelays the spring bloom. The chlorophyll gradient in the middlelayer has a large impact on the response of the model to short-termvariability in the meteorological forcings.     

Recent climate hiatus revealed dual control by temperature and drought on the stem growth of Mediterranean Quercus ilex

A better understanding of stem growth phenology and its climate drivers would improve projections of the impact of climate change on forest productivity. Under a Mediterranean climate, tree growth is primarily limited by soil water availability during summer, but cold temperatures in winter also prevent tree growth in evergreen forests. In the widespread Mediterranean evergreen tree species Quercus ilex, the duration of stem growth has been shown to predict annual stem increment, and to be limited by winter temperatures on the one hand, and by the summer drought onset on the other hand. We tested how these climatic controls of Q. ilex growth varied with recent climate change by correlating a 40‐year tree ring record and a 30‐year annual diameter inventory against winter temperature, spring precipitation, and simulated growth duration. Our results showed that growth duration was the best predictor of annual tree growth. We predicted that recent climate changes have resulted in earlier growth onset (?10 days) due to winter warming and earlier growth cessation (?26 days) due to earlier drought onset. These climatic trends partly offset one another, as we observed no significant trend of change in tree growth between 1968 and 2008. A moving‐window correlation analysis revealed that in the past, Q. ilex growth was only correlated with water availability, but that since the 2000s, growth suddenly became correlated with winter temperature in addition to spring drought. This change in the climate–growth correlations matches the start of the recent atmospheric warming pause also known as the ‘climate hiatus’. The duration of growth of Q. ilex is thus shortened because winter warming has stopped compensating for increasing drought in the last decade. Decoupled trends in precipitation and temperature, a neglected aspect of climate change, might reduce forest productivity through phenological constraints and have more consequences than climate warming alone.     

The influence of climate on the timing and rate of spring bird migration

Ecological processes are changing in response to climatic warming. Birds, in particular, have been documented to arrive and breed earlier in spring and this has been attributed to elevated spring temperatures. It is not clear, however, how long-distance migratory birds that overwinter thousands of kilometers to the south in the tropics cue into changes in temperature or plant phenology on northern breeding areas. We explored the relationships between the timing and rate of spring migration of long-distance migratory birds, and variables such as temperature, the North Atlantic Oscillation (NAO) and plant phenology, using mist net capture data from three ringing stations in North America over a 40-year period. Mean April/May temperatures in eastern North America varied over a 5°C range, but with no significant trend during this period. Similarly, we found few significant trends toward earlier median capture dates of birds. Median capture dates were not related to the NAO, but were inversely correlated to spring temperatures for almost all species. For every 1°C increase in spring temperature, median capture dates of migratory birds averaged, across species, one day earlier. Lilac (Syringa vulgaris) budburst, however, averaged 3 days earlier for every 1°C increase in spring temperature, suggesting that the impact of temperature on plant phenology is three times greater than on bird phenology. To address whether migratory birds adjust their rate of northward migration to changes in temperature, we compared median capture dates for 15 species between a ringing station on the Gulf Coast of Louisiana in the southern USA with two stations approximately 2,500 km to the north. The interval between median capture dates in Louisiana and at the other two ringing stations was inversely correlated with temperature, with an average interval of 22 days, that decreased by 0.8 days per 1°C increase in temperature. Our results suggest that, although the onset of migration may be determined endogenously, the timing of migration is flexible and can be adjusted in response to variation in weather and/or phenology along migration routes.     

Phytoplankton response to a changing climate

Phytoplankton are at the base of aquatic food webs and of global importance for ecosystem functioning and services. The dynamics of these photosynthetic cells are linked to annual fluctuations of temperature, water column mixing, resource availability, and consumption. Climate can modify these environmental factors and alter phytoplankton structure, seasonal dynamics, and taxonomic composition. Here, we review mechanistic links between climate alterations and factors limiting primary production, and highlight studies where climate change has had a clear impact on phytoplankton processes. Climate affects phytoplankton both directly through physiology and indirectly by changing water column stratification and resource availability, mainly nutrients and light, or intensified grazing by heterotrophs. These modifications affect various phytoplankton processes, and a widespread advance in phytoplankton spring bloom timing and changing bloom magnitudes have both been observed. Climate warming also affects phytoplankton species composition and size structure, and favors species traits best adapted to changing conditions associated with climate change. Shifts in phytoplankton can have far-reaching consequences for ecosystem structure and functioning. An improved understanding of the mechanistic links between climate and phytoplankton dynamics is important for predicting climate change impacts on aquatic ecosystems.     

Oceanographic drivers and mistiming processes shape breeding success in a seabird

Understanding the processes driving seabirds'' reproductive performance through trophic interactions requires the identification of seasonal pulses in marine productivity. We investigated the sequence of environmental and biological processes driving the reproductive phenology and performance of the storm petrel (Hydrobates pelagicus) in the Western Mediterranean. The enhanced light and nutrient availability at the onset of water stratification (late winter/early spring) resulted in annual consecutive peaks in relative abundance of phytoplankton, zooplankton and ichthyoplankton. The high energy-demanding period of egg production and chick rearing coincided with these successive pulses in food availability, pointing to a phenological adjustment to such seasonal patterns with important fitness consequences. Indeed, delayed reproduction with respect to the onset of water stratification resulted in both hatching and breeding failure. This pattern was observed at the population level, but also when confounding factors such as individuals'' age or experience were also accounted for. We provide the first evidence of oceanographic drivers leading to the optimal time-window for reproduction in an inshore seabird at southern European latitudes, along with a suitable framework for assessing the impact of environmentally driven changes in marine productivity patterns in seabird performance.