John A. Lindley

Synergistic Effects of Climate and Fishing in a Marine Ecosystem

Current climate change and overfishing are affecting the productivity and structure of marine ecosystems. This situation is unprecedented for the marine biosphere and it is essential to understand the mechanisms and pathways by which ecosystems respond. We report that climate change and overfishing are likely to be responsible for a rapid restructuring of a highly productive marine ecosystem with effects throughout the pelagos and the benthos. In the mid-1980s, climate change, consequent modifications in the North Sea plankton, and fishing, all reduced North Sea cod recruitment. In this region, production of many benthic species respond positively and immediately to temperature. Analysis of a long-term, spatially extensive biological (plankton and cod) and physical (sea surface temperature) dataset suggests that synchronous changes in cod numbers and sea temperature have established an extensive trophic cascade favoring lower trophic level groups over economic fisheries. A proliferation of jellyfish that we detect may signal the climax of these changes. This modified North Sea ecology may provide a clear indication of the synergistic consequences of coincident climate change and overfishing. The extent of the ecosystem restructuring that has occurred in the North Sea suggests we are unlikely to reverse current climate and human-induced effects through ecosystem resource management in the short term. Rather, we should understand and adapt to new ecological regimes. This implies that fisheries management policies will have to be fully integrated with the ecological consequences of climate change to prevent a similar collapse in an exploited marine ecosystem elsewhere.

Fathers in hot water: rising sea temperatures and a Northeastern Atlantic pipefish baby boom

We report unprecedented numbers of juvenile snake pipefish, Entelurus aequoreus, in continuous plankton records of the Northeastern Atlantic since 2002. Increased sea surface temperatures (SSTs) in the Northern Hemisphere, linked to global warming, are a likely cause. Analysis of a long-term time-series of SST data in the Northeastern Atlantic shows a rise in winter, spring and summer sea temperatures (January–September), when the eggs of E. aqueoreus, which are brooded by the male, are developing and the larvae are growing in plankton. From what is known of the reproductive biology of closely related species, we suggest that the increased abundance of larval and juvenile E. aequoreus in the plankton as far west as the Mid-Atlantic Ridge may reflect the impact of temperature on abundance, through its effects on the operational sex ratio and potential reproductive rate, the onset of the breeding season and juvenile survival in this sex role reversed fish.

Molecular analysis of Continuous Plankton Recorder samples, an examination of echinoderm larvae in the North Sea

Analysis of the biological time series of plankton samples collected by the Continuous Plankton Recorder (CPR) in the North Atlantic and North Sea has shown a regime shift in the plankton in this region. Both the distributions of planktonic organisms and their timing of occurrence in the seasonal cycle have changed and these changes appear to ref lect global warming. In the North Sea the planktonic larvae of echinoderms have shown a recent dramatic increase in both relative and absolute abundance and their seasonal peak of occurrence has advanced by 47 days. The identity of the echinoderm larvae involved in this change has, however, remained equivocal. The small size of many organisms like echinoderm larvae combined with incomplete taxonomic keys hinders their visual identification and their fragility often means that useful morphological features are damaged during sampling by the CPR. Here, using new molecular methods applied to CPR samples, we show that planktonic larvae of the benthic Echinocardium cordatum dominate the North Sea plankton. We argue that since this species benefits from mild winters and warmer waters their numerical increase in the plankton is consistent with recent climatic changes that appear to be affecting the wider ecology of this region.

North Sea ecosystem change from swimming crabs to seagulls.

A recent increase in sea temperature has established a new ecosystem dynamic regime in the North Sea. Climate-induced changes in decapods have played an important role. Here, we reveal a coincident increase in the abundance of swimming crabs and lesser black-backed gull colonies in the North Sea, both in time and in space. Swimming crabs are an important food source for lesser black-backed gulls during the breeding season. Inhabiting the land, but feeding mainly at sea, lesser black-backed gulls provide a link between marine and terrestrial ecosystems, since the bottom-up influence of allochthonous nutrient input from seabirds to coastal soils can structure the terrestrial food web. We, therefore, suggest that climate-driven changes in trophic interactions in the marine food web may also have ensuing ramifications for the coastal ecology of the North Sea.

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.

Population dynamics in lesser black- backed gulls in the Netherlands support a North Sea regime shift

Shamoun-Baranes & Camphuysen [1] made two main points in their critical appraisal of our recent article [2]: (i) that the Larus fuscus population increased in the Netherlands well before a mid 1980s regime shift in the North Sea and (ii) that population increases based on a simple prey type are difficult to imagine. These two comments give us the opportunity to deepen and complete our conclusions. Before we consider them, however, it is important to note that Shamoun-Baranes & Camphuysen [1] present conclusions outside the time window considered in our study, focus only on the Netherlands, and do not give any analysis of population trends. With respect to the first point—that the L. fuscus population increased in the Netherlands well before a mid 1980s North Sea regime shift—it is important to highlight that the regime shift we referred to occurred in the mid-1990s. As our figure 2 [2] indicates clearly, the gull colonies in the Netherlands changed little during our study period from 1986 to 2000. Consequently, the first point made by Shamoun-Baranes & Camphuysen [1] has to be viewed as an idiosyncratic characteristic when considering spatial heterogeneity as a fundamental ecological property in ecosystem functioning [3], for which our analysis of gull populations in the broader North Sea region, allowed. With respect to the second point—that population increases based on a simple prey type are difficult to imagine—Shamoun-Baranes & Camphuysen [1] support their argument with the observation that crustaceans have much lower energy value than fishes, which represented around 80 per cent of the gulls diet by mass. While we agree (even though we did not find these results in their cited reference [4]), the same study [4] reports that the swimming crab Liocarcinus holsatus is the third most important prey for L. fuscus in the Texel colony (20% in the 2005–2010 period), confirming de facto part of our findings. As shown by several authors [5,6], seabirds may be influenced by changes in both food quantity and quality, and they may affect different components of reproduction and survival: for example, fledging success (survival from hatching to fledging) shows a positive relationship with food quality, but not with food quantity [5]. In this regard, Shamoun-Baranes & Camphuysen [1] omitted to mention a key study by Schwemmer & Garthe [7], which showed that swimming crabs—Liocarcinus sp.—were a major dietary item during both the egg-stage and the chick-rearing period, when the number of breeding pairs of L. fuscus were increasing exponentially along the German coast in the 1990s (figure 2 in [2]). During the breeding season, birds require specific nutrients in their diet [8] and Schwemmer & Garthe [7] suggested that swimming crabs—Liocarcinus sp.—may be a valuable source of calcium for both eggshells and the bone development of chicks. Interestingly, the observations by Schwemmer and Garthe may have also provided an answer to Camphuysen [9], who concluded that the foraging range of L. fuscus further out to sea could not be explained fully by either a change in the abundance of fishing vessels or the avoidance of herring gulls (Larus argentatus), and that it must, therefore, involve another unknown offshore food resource. Shamoun-Baranes & Camphuysen [1] only referred to their own local study [9] on the importance of fishing discards in the gulls diets, whereas swimming crabs found in the L. fuscuss diet are obtained by natural feeding [4,7]. One hypothesis proposed by Schwemmer & Garthe [7] to support their findings was an increase in the abundance of Liocarcinus sp., which we confirmed in our study [2]. To conclude, the observations of Shamoun-Baranes & Camphuysen [1] on a single population of L. fuscus from the Netherlands most likely indicate that they were at the wrong place (idiosyncratic results owing to spatial scaling and heterogeneity), at the wrong time period (ante 1989), while also failing to consider food quality as an important parameter in food selection. Although Lindley et al. [10] showed that the increase in decapods (dominated by swimming crabs of the sub-family Polybiinae) was a key component of the trophic amplification of hydroclimatic change and the development of a new North Sea ecosystem dynamic regime [11,12], we do agree with Shamoun-Baranes & Camphuysen [1] that a deeper exploration of the drivers influencing gull population dynamics at several spatial and temporal scales is needed, as it is for any complex adaptive system.