Comparative analysis of European wide marine ecosystem shifts: a large-scale approach for developing the basis for ecosystem-based management

Abrupt and rapid ecosystem shifts (where major reorganizations of food-web and community structures occur), commonly termed regime shifts, are changes between contrasting and persisting states of ecosystem structure and function. These shifts have been increasingly reported for exploited marine ecosystems around the world from the North Pacific to the North Atlantic. Understanding the drivers and mechanisms leading to marine ecosystem shifts is crucial in developing adaptive management strategies to achieve sustainable exploitation of marine ecosystems. An international workshop on a comparative approach to analysing these marine ecosystem shifts was held at Hamburg University, Institute for Hydrobiology and Fisheries Science, Germany on 1-3 November 2010. Twenty-seven scientists from 14 countries attended the meeting, representing specialists from seven marine regions, including the Baltic Sea, the North Sea, the Barents Sea, the Black Sea, the Mediterranean Sea, the Bay of Biscay and the Scotian Shelf off the Canadian East coast. The goal of the workshop was to conduct the first large-scale comparison of marine ecosystem regime shifts across multiple regional areas, in order to support the development of ecosystem-based management strategies.     

Causes and projections of abrupt climate-driven ecosystem shifts in the North Atlantic

Warming of the global climate is now unequivocal and its impact on Earth' functional units has become more apparent. Here, we show that marine ecosystems are not equally sensitive to climate change and reveal a critical thermal boundary where a small increase in temperature triggers abrupt ecosystem shifts seen across multiple trophic levels. This large-scale boundary is located in regions where abrupt ecosystem shifts have been reported in the North Atlantic sector and thereby allows us to link these shifts by a global common phenomenon. We show that these changes alter the biodiversity and carrying capacity of ecosystems and may, combined with fishing, precipitate the reduction of some stocks of Atlantic cod already severely impacted by exploitation. These findings offer a way to anticipate major ecosystem changes and to propose adaptive strategies for marine exploited resources such as cod in order to minimize social and economic consequences.     

Climate and ecosystem linkages explain widespread declines in North American Atlantic salmon populations

North American Atlantic salmon (Salmo salar) populations experienced substantial declines in the early 1990s, and many populations have persisted at low abundances in recent years. Abundance and productivity declined in a coherent manner across major regions of North America, and this coherence points toward a potential shift in marine survivorship, rather than local, river‐specific factors. The major declines in Atlantic salmon populations occurred against a backdrop of physical and biological shifts in Northwest Atlantic ecosystems. Analyses of changes in climate, physical, and lower trophic level biological factors provide substantial evidence that climate conditions directly and indirectly influence the abundance and productivity of North American Atlantic salmon populations. A major decline in salmon abundance after 1990 was preceded by a series of changes across multiple levels of the ecosystem, and a subsequent population change in 1997, primarily related to salmon productivity, followed an unusually low NAO event. Pairwise correlations further demonstrate that climate and physical conditions are associated with changes in plankton communities and prey availability, which are ultimately linked to Atlantic salmon populations. Results suggest that poor trophic conditions, likely due to climate‐driven environmental factors, and warmer ocean temperatures throughout their marine habitat area are constraining the productivity and recovery of North American Atlantic salmon populations.     

Marine biological shifts and climate

Phenological, biogeographic and community shifts are among the reported responses of marine ecosystems and their species to climate change. However, despite both the profound consequences for ecosystem functioning and services, our understanding of the root causes underlying these biological changes remains rudimentary. Here, we show that a significant proportion of the responses of species and communities to climate change are deterministic at some emergent spatio-temporal scales, enabling testable predictions and more accurate projections of future changes. We propose a theory based on the concept of the ecological niche to connect phenological, biogeographic and long-term community shifts. The theory explains approximately 70% of the phenological and biogeographic shifts of a key zooplankton Calanus finmarchicus in the North Atlantic and approximately 56% of the long-term shifts in copepods observed in the North Sea during the period 1958–2009.     

Regime shifts of Mediterranean forest carbon uptake and reduced resilience driven by multidecadal ocean surface temperatures

The mechanisms translating global circulation changes into rapid abrupt shifts in forest carbon capture in semi‐arid biomes remain poorly understood. Here, we report unprecedented multidecadal shifts in forest carbon uptake in semi‐arid Mediterranean pine forests in Spain over 1950–2012. The averaged carbon sink reduction varies between 31% and 37%, and reaches values in the range of 50% in the most affected forest stands. Regime shifts in forest carbon uptake are associated with climatic early warning signals, decreased forest regional synchrony and reduced long‐term carbon sink resilience. We identify the mechanisms linked to ocean multidecadal variability that shape regime shifts in carbon capture. First, we show that low‐frequency variations of the surface temperature of the Atlantic Ocean induce shifts in the non‐stationary effects of El Niño Southern Oscillation (ENSO) on regional forest carbon capture. Modelling evidence supports that the non‐stationary effects of ENSO can be propagated from tropical areas to semi‐arid Mediterranean biomes through atmospheric wave trains. Second, decadal changes in the Atlantic Multidecadal Oscillation (AMO) significantly alter sea–air heat exchanges, modifying in turn ocean vapour transport over land and land surface temperatures, and promoting sustained drought conditions in spring and summer that reduce forest carbon uptake. Third, we show that lagged effects of AMO on the winter North Atlantic Oscillation also contribute to the maintenance of long‐term droughts. Finally, we show that the reported strong, negative effects of ocean surface temperature (AMO) on forest carbon uptake in the last decades are unprecedented over the last 150 years. Our results provide new, unreported explanations for carbon uptake shifts in these drought‐prone forests and review the expected impacts of global warming on the profiled mechanisms.     

Rapid biogeographical plankton shifts in the North Atlantic Ocean

Large‐scale biogeographical changes in the biodiversity of a key zooplankton group (calanoid copepods) were detected in the north‐eastern part of the North Atlantic Ocean and its adjacent seas over the period 1960–1999. These findings provided key empirical evidence for climate change impacts on marine ecosystems at the regional to oceanic scale. Since 1999, global temperatures have continued to rise in the region. Here, we extend the analysis to the period 1958–2005 using all calanoid copepod species assemblages (nine species assemblages based on an analysis including a total of 108 calanoid species or taxa) and show that this phenomenon has been reinforced in all regions. Our study reveals that the biodiversity of calanoid copepods are responding quickly to sea surface temperature (SST) rise by moving geographically northward at a rapid rate up to about 23.16 km yr^?1. Our analysis suggests that nearly half of the increase in sea temperature in the northeast Atlantic and adjacent seas is related to global temperature rises (46.35% of the total variance of temperature) while changes in both natural modes of atmospheric and oceanic circulation explain 26.45% of the total variance of temperature. Although some SST isotherms have moved northwards by an average rate of up to 21.75 km yr^?1 (e.g. the North Sea), their movement cannot fully quantify all species assemblage shifts. Furthermore, the observed rates of biogeographical movements are far greater than those observed in the terrestrial realm. Here, we discuss the processes that may explain such a discrepancy and suggest that the differences are mainly explained by the fluid nature of the pelagic domain, the life cycle of the zooplankton and the lesser anthropogenic influence (e.g. exploitation, habitat fragmentation) on these organisms. We also hypothesize that despite changes in the path and intensity of the oceanic currents that may modify quickly and greatly pelagic zooplankton species, these organisms may reflect better the current impact of climate warming on ecosystems as terrestrial organisms are likely to significantly lag the current impact of climate change.     

Large species shifts triggered by small forces

Changes in species composition of communities seem to proceed gradually at first sight, but remarkably rapid shifts are known to occur. Although disrupting disturbances seem an obvious explanation for such shifts, evidence for large disturbances is not always apparent. Here we show that complex communities tend to move through occasional catastrophic shifts in response to gradual environmental change or evolution. This tendency is caused by multiple attractors that may exist in such systems. We show that alternative attractors arise robustly in randomly generated multispecies models, especially if competition is symmetrical and if interspecific competition is allowed to exceed intraspecific competition. Inclusion of predators as a second trophic level did not alter the results greatly, although it reduced the probability of alternative attractors somewhat. These results suggest that alternative attractors may commonly arise from interactions between large numbers of species. Consequently, the response of complex communities to environmental change is expected to be characterized by hysteresis and sudden shifts. Some unexplained regime shifts observed in ecosystems could be related to alternative attractors arising from complex species interactions. Additionally, our results support the idea that ancient mass extinctions may partly be due to an intrinsic loss of stability of species configurations.     

Marine Ecosystem Response to the Atlantic Multidecadal Oscillation

Against the backdrop of warming of the Northern Hemisphere it has recently been acknowledged that North Atlantic temperature changes undergo considerable variability over multidecadal periods. The leading component of natural low-frequency temperature variability has been termed the Atlantic Multidecadal Oscillation (AMO). Presently, correlative studies on the biological impact of the AMO on marine ecosystems over the duration of a whole AMO cycle (∼60 years) is largely unknown due to the rarity of continuously sustained biological observations at the same time period. To test whether there is multidecadal cyclic behaviour in biological time-series in the North Atlantic we used one of the world''s longest continuously sustained marine biological time-series in oceanic waters, long-term fisheries data and historical records over the last century and beyond. Our findings suggest that the AMO is far from a trivial presence against the backdrop of continued temperature warming in the North Atlantic and accounts for the second most important macro-trend in North Atlantic plankton records; responsible for habitat switching (abrupt ecosystem/regime shifts) over multidecadal scales and influences the fortunes of various fisheries over many centuries.     

Sleeping functional group drives coral-reef recovery

The world's coral reefs are in decline, with many exhibiting a phase shift from coral to macroalgal dominance . This change is often associated with habitat loss and overharvesting of herbivorous fishes, particularly parrotfishes and surgeonfishes . The challenge is to reverse this decline and enhance the resilience of coral-reef ecosystems . We demonstrate, by using a large-scale experimentally induced phase shift, that the rapid reversal from a macroalgal-dominated to a coral- and epilithic algal-dominated state was not a result of herbivory by parrotfishes or surgeonfishes. Surprisingly, phase-shift reversal was primarily driven by a single batfish species (Platax pinnatus), a fish previously regarded as an invertebrate feeder. The 43 herbivorous fishes in the local fauna played only a minor role, suggesting that biodiversity may not offer the protection we hoped for in complex ecosystems. Our findings highlight the dangers faced by coral reefs and other threatened complex ecosystems: Species or functional groups that prevent phase shifts may not be able to reverse phase shifts once they occur. Nevertheless, reversal is possible. The critical issue is to identify and protect those groups that underpin the resilience and regeneration of complex ecosystems.     

The future of the northeast Atlantic benthic flora in a high CO2 world

Seaweed and seagrass communities in the northeast Atlantic have been profoundly impacted by humans, and the rate of change is accelerating rapidly due to runaway CO₂ emissions and mounting pressures on coastlines associated with human population growth and increased consumption of finite resources. Here, we predict how rapid warming and acidification are likely to affect benthic flora and coastal ecosystems of the northeast Atlantic in this century, based on global evidence from the literature as interpreted by the collective knowledge of the authorship. We predict that warming will kill off kelp forests in the south and that ocean acidification will remove maerl habitat in the north. Seagrasses will proliferate, and associated epiphytes switch from calcified algae to diatoms and filamentous species. Invasive species will thrive in niches liberated by loss of native species and spread via exponential development of artificial marine structures. Combined impacts of seawater warming, ocean acidification, and increased storminess may replace structurally diverse seaweed canopies, with associated calcified and noncalcified flora, with simple habitats dominated by noncalcified, turf‐forming seaweeds.     

Regime Shifts in the Anthropocene: Drivers,Risks, and Resilience

Many ecosystems can experience regime shifts: surprising, large and persistent changes in the function and structure of ecosystems. Assessing whether continued global change will lead to further regime shifts, or has the potential to trigger cascading regime shifts has been a central question in global change policy. Addressing this issue has, however, been hampered by the focus of regime shift research on specific cases and types of regime shifts. To systematically assess the global risk of regime shifts we conducted a comparative analysis of 25 generic types of regime shifts across marine, terrestrial and polar systems; identifying their drivers, and impacts on ecosystem services. Our results show that the drivers of regime shifts are diverse and co-occur strongly, which suggests that continued global change can be expected to synchronously increase the risk of multiple regime shifts. Furthermore, many regime shift drivers are related to climate change and food production, whose links to the continued expansion of human activities makes them difficult to limit. Because many regime shifts can amplify the drivers of other regime shifts, continued global change can also be expected to increase the risk of cascading regime shifts. Nevertheless, the variety of scales at which regime shift drivers operate provides opportunities for reducing the risk of many types of regime shifts by addressing local or regional drivers, even in the absence of rapid reduction of global drivers.     

Predators of northern shrimp, Pandalus borealis (Pandalidae), throughout the North Atlantic

A compendium of northern shrimp (Pandalus borealis) predators was assembled, thereby consolidating decades of research that described trophic interactions among relevant marine species in the North Atlantic. The importance of shrimp as prey and the impacts of predation on shrimp populations were gleaned, where possible, from the literature. The review identified 26 species that prey on shrimp within North Atlantic ecosystems. The results clarified the role of shrimp as prey within these ecosystems, confirming that they provide an abundant source of food for marine fish, mammals and invertebrates throughout the North Atlantic. The evidence supported the likelihood of predation mortality as one of the key factors regulating shrimp population dynamics. However, lacking representative estimates of shrimp consumption by predators, the net effect on predation mortality within populations was unquantifiable.     

Variability in the mean latitude of the Atlantic Intertropical Convergence Zone as recorded by riverine input of sediments to the Cariaco Basin (Venezuela)

Changes in the strength and position of the Intertropical Convergence Zone (ITCZ) are an important component of climate variability in the tropical Atlantic. The Cariaco Basin, located on the northern margin of Venezuela, is sensitive to tropical Atlantic climate change and its sediments provide a record of past ITCZ behavior. Today, the Cariaco Basin experiences two distinct seasons that reflect the annual migration of the Atlantic ITCZ. Between January and March, when the ITCZ lies south of the equator, northeasterly trade winds sit directly over Cariaco Basin and strong coastal upwelling and dry conditions dominate. Beginning in June-July, as the ITCZ moves north, local rainfall reaches a maximum and the upwelling diminishes or disappears. Here we summarize new and previously published data on the river-derived terrigenous fraction of Cariaco Basin sediments, as well as comparisons to other paleoclimate records, which together suggest a coherent climatologic response in the tropical Atlantic triggered by a pattern of ITCZ migration that mimics the seasonal cycle. During periods of cooler North Atlantic SSTs, on time-scales ranging from the Little Ice Age to the Younger Dryas to the cold stadials of the last glacial, decreased detrital delivery to Cariaco Basin from local rivers suggests a southward shift in the mean latitudinal position of the ITCZ. During warm interstadials and periods of Holocene and deglacial warmth, northward shifts in ITCZ position and its belt of convective rainfall are inferred from increased detrital delivery to the basin. Whether the rapid shifts in ITCZ position and precipitation recorded by Cariaco Basin sediments and other regional records reflect a response to forcing originating in the high latitude Atlantic or to forcing potentially sourced in the tropics is a key question yet to be fully answered.     

Genetically based adaptive trait shifts at an expanding mangrove range margin

Hydrobiologia - Neotropical black mangrove (Avicennia germinans) is expanding poleward into temperate salt marsh along Atlantic Florida, USA, with field evidence of trait shifts consistent with...     

Evidence of climate‐driven ecosystem reorganization in the Gulf of Mexico

The Gulf of Mexico is one of the most ecologically and economically valuable marine ecosystems in the world and is affected by a variety of natural and anthropogenic phenomena including climate, hurricanes, coastal development, agricultural runoff, oil spills, and fishing. These complex and interacting stressors, together with the highly dynamic nature of this ecosystem, present challenges for the effective management of its resources. We analyze a compilation of over 100 indicators representing physical, biological, and economic aspects of the Gulf of Mexico and find that an ecosystem‐wide reorganization occurred in the mid‐1990s. Further analysis of fishery landings composition data indicates a major shift in the late 1970s coincident with the advent of US national fisheries management policy, as well as significant shifts in the mid‐1960s and the mid‐1990s. These latter shifts are aligned temporally with changes in a major climate mode in the Atlantic Ocean: the Atlantic Multidecadal Oscillation (AMO). We provide an explanation for how the AMO may drive physical changes in the Gulf of Mexico, thus altering higher‐level ecosystem dynamics. The hypotheses presented here should provide focus for further targeted studies, particularly in regard to whether and how management should adjust to different climate regimes or states of nature. Our study highlights the challenges in understanding the effects of climatic drivers against a background of multiple anthropogenic pressures, particularly in a system where these forces interact in complex and nonlinear ways.     

Rapid adaptation in a fast-changing world: Emerging insights from insect genomics

Many researchers have questioned the ability of biota to adapt to rapid anthropogenic environmental shifts. Here, we synthesize emerging genomic evidence for rapid insect evolution in response to human pressure. These new data reveal diverse genomic mechanisms (single locus, polygenic, structural shifts; introgression) underpinning rapid adaptive responses to a variety of anthropogenic selective pressures. While the effects of some human impacts (e.g. pollution; pesticides) have been previously documented, here we highlight startling new evidence for rapid evolutionary responses to additional anthropogenic processes such as deforestation. These recent findings indicate that diverse insect assemblages can indeed respond dynamically to major anthropogenic evolutionary challenges. Our synthesis also emphasizes the critical roles of genomic architecture, standing variation and gene flow in maintaining future adaptive potential. Broadly, it is clear that genomic approaches are essential for predicting, monitoring and responding to ongoing anthropogenic biodiversity shifts in a fast-changing world.     

Cascading effects of climate extremes on vertebrate fauna through changes to low‐latitude tree flowering and fruiting phenology

Forest vertebrate fauna provide critical services, such as pollination and seed dispersal, which underpin functional and resilient ecosystems. In turn, many of these fauna are dependent on the flowering phenology of the plant species of such ecosystems. The impact of changes in climate, including climate extremes, on the interaction between these fauna and flora has not been identified or elucidated, yet influences on flowering phenology are already evident. These changes are well documented in the mid to high latitudes. However, there is emerging evidence that the flowering phenology, nectar/pollen production, and fruit production of long‐lived trees in tropical and subtropical forests are also being impacted by changes in the frequency and severity of climate extremes. Here, we examine the implications of these changes for vertebrate fauna dependent on these resources. We review the literature to establish evidence for links between climate extremes and flowering phenology, elucidating the nature of relationships between different vertebrate taxa and flowering regimes. We combine this information with climate change projections to postulate about the likely impacts on nectar, pollen and fruit resource availability and the consequences for dependent vertebrate fauna. The most recent climate projections show that the frequency and intensity of climate extremes will increase during the 21st century. These changes are likely to significantly alter mass flowering and fruiting events in the tropics and subtropics, which are frequently cued by climate extremes, such as intensive rainfall events or rapid temperature shifts. We find that in these systems the abundance and duration of resource availability for vertebrate fauna is likely to fluctuate, and the time intervals between episodes of high resource availability to increase. The combined impact of these changes has the potential to result in cascading effects on ecosystems through changes in pollinator and seed dispersal ecology, and demands a focused research effort.     

Evolutionary regime shifts in simulated ecosystems

Catastrophic regime shifts in ecosystems occur when the system is tipped into a new attractor state under some external forcing. Here we consider whether evolutionary adaptations within ecosystems can trigger similar transitions. We use an individual‐based, evolutionary model of interconnected ecosystems to analyze nonlinear changes in global state resulting from local adaptations. Transitions between periods of stability occur when new traits arise that allow exploitation of under‐utilized resources. Subsequent rapid growth of the population carrying the new trait causes abrupt environmental change that drives incumbent species extinct. We call these transitions ‘evolutionary regime shifts’. These internally generated perturbations can result in ecosystem collapse, followed by recovery to an alternate stable state, or occasionally system‐wide extinction. While these disruptions may have a negative impact on ecosystem productivity in individual simulation runs, mean results over many simulations show a trend for increasing ecosystem productivity and stability over time. Feedback between life and the abiotic environment in the model creates a ‘long‐tailed’ distribution of extinction sizes without any external trigger for large extinction events.     

Anthropogenic evolution in an insect wing polymorphism following widespread deforestation

Anthropogenic environmental change can underpin major shifts in natural selective regimes, and can thus alter the evolutionary trajectories of wild populations. However, little is known about the evolutionary impacts of deforestation—one of the most pervasive human-driven changes to terrestrial ecosystems globally. Absence of forest cover (i.e. exposure) has been suggested to play a role in selecting for insect flightlessness in montane ecosystems. Here, we capitalize on human-driven variation in alpine treeline elevation in New Zealand to test whether anthropogenic deforestation has caused shifts in the distributions of flight-capable and flightless phenotypes in a wing-polymorphic lineage of stoneflies from the Zelandoperla fenestrata species complex. Transect sampling revealed sharp transitions from flight-capable to flightless populations with increasing elevation. However, these phenotypic transitions were consistently delineated by the elevation of local treelines, rather than by absolute elevation, providing a novel example of human-driven evolution in response to recent deforestation. The inferred rapid shifts to flightlessness in newly deforested regions have implications for the evolution and conservation of invertebrate biodiversity.     

Trophic plasticity in the Atlantic sharpnose shark (Rhizoprionodon terraenovae) from the north central Gulf of Mexico

Quantifying the trophic role of sharks in coastal ecosystems is crucial for the construction of accurate ecosystem models. This is particularly important for wide-ranging species like the Atlantic sharpnose shark (Rhizoprionodon terraenovae), ubiquitous across the northern Gulf of Mexico. We used gut content and stable isotope analyses to determine if differences in abundance of Atlantic sharpnose sharks in the waters around Mobile Bay, Alabama translated into differences in dietary sources or trophic position among sharks sampled east and west relative to the mouth of the bay. Gut content analysis suggested that Atlantic sharpnose sharks eat primarily teleost fishes (%IRI?>?90% across size classes), and both stomach content and stable isotope analyses highlighted an ontogenetic shift in diet. Nitrogen stable isotope data from liver and muscle tissues indicated regional shifts in trophic position for Atlantic sharpnose sharks. The mixing model SIAR (stable isotope analysis in R) v.4.0.2 was used to suggest possible contributions from likely prey items for Atlantic sharpnose sharks sampled east and west of Mobile Bay. Portunid crabs and shrimp made higher contributions to the diet of Atlantic sharpnose sharks in the western region, compared to higher and more variable contributions from fish like croaker (Micropogonias undulatus) and hardhead catfish (Arius felis) in the eastern region. Our results suggest trophic plasticity in Atlantic sharpnose sharks, findings that emphasize the importance of examining regional variation in trophic position when constructing coastal foodweb models.