Recurrent jellyfish blooms are a consequence of global oscillations.

A perceived recent increase in global jellyfish abundance has been portrayed as a symptom of degraded oceans. This perception is based primarily on a few case studies and anecdotal evidence, but a formal analysis of global temporal trends in jellyfish populations has been missing. Here, we analyze all available long-term datasets on changes in jellyfish abundance across multiple coastal stations, using linear and logistic mixed models and effect-size analysis to show that there is no robust evidence for a global increase in jellyfish. Although there has been a small linear increase in jellyfish since the 1970s, this trend was unsubstantiated by effect-size analysis that showed no difference in the proportion of increasing vs. decreasing jellyfish populations over all time periods examined. Rather, the strongest nonrandom trend indicated jellyfish populations undergo larger, worldwide oscillations with an approximate 20-y periodicity, including a rising phase during the 1990s that contributed to the perception of a global increase in jellyfish abundance. Sustained monitoring is required over the next decade to elucidate with statistical confidence whether the weak increasing linear trend in jellyfish after 1970 is an actual shift in the baseline or part of an oscillation. Irrespective of the nature of increase, given the potential damage posed by jellyfish blooms to fisheries, tourism, and other human industries, our findings foretell recurrent phases of rise and fall in jellyfish populations that society should be prepared to face.

Negative and positive interspecific interactions involving jellyfish polyps in marine sessile communities.

Sessile marine invertebrates on hard substrates are one of the two canonical examples of communities structured by competition, but some aspects of their dynamics remain poorly understood. Jellyfish polyps are an important but under-studied component of these communities. We determined how jellyfish polyps interact with their potential competitors in sessile marine hard-substrate communities, using a combination of experiments and modelling. We carried out an experimental study of the interaction between polyps of the moon jellyfish Aurelia aurita and potential competitors on settlement panels, in which we determined the effects of reduction in relative abundance of either A. aurita or potential competitors at two depths. We predicted that removal of potential competitors would result in a relative increase in A. aurita that would not depend on depth, and that removal of A. aurita would result in a relative increase in potential competitors that would be stronger at shallower depths, where oxygen is less likely to be limiting. Removal of potential competitors resulted in a relative increase in A. aurita at both depths, as predicted. Unexpectedly, removal of A. aurita resulted in a relative decrease in potential competitors at both depths. We investigated a range of models of competition for space, of which the most successful involved enhanced overgrowth of A. aurita by potential competitors, but none of these models was completely able to reproduce the observed pattern. Our results suggest that interspecific interactions in this canonical example of a competitive system are more complex than is generally believed.

Jellyfish life histories: role of polyps in forming and maintaining scyphomedusa populations.

Large population fluctuations of jellyfish occur over a variety of temporal scales, from weekly to seasonal, inter-annual and even decadal, with some regions of the world reported to be experiencing persistent seasonal bloom events. Recent jellyfish research has focussed on understanding the causes and consequences of these population changes, with the vast majority of studies considering the effect of changing environmental variables only on the pelagic medusa. But many of the bloom-forming species are members of the Scyphozoa with complex metagenic life cycles consisting of a sexually reproducing pelagic medusa and asexually reproducing benthic polyp. Recruitment success during the juvenile (planula, polyp and ephyrae) stages of the life cycle can have a major effect on the abundance of the adult (medusa) population, but until very recently, little was known about the ecology of the polyp or scyphistoma phase of the scyphozoan life cycle. The aim of this review is to synthesise the current state of knowledge of polyp ecology by examining (1) the recruitment and metamorphosis of planulae larvae into polyps, (2) survival and longevity of polyps, (3) expansion of polyp populations via asexual propagation and (4) strobilation and recruitment of ephyrae (juvenile medusae). Where possible, comparisons are made with the life histories of other bentho-pelagic marine invertebrates so that further inferences can be made. Differences between tropical and temperate species are highlighted and related to climate change, and populations of the same species (in particular Aurelia aurita) inhabiting different habitats within its geographic range are compared. The roles that polyps play in ensuring the long-term survival of jellyfish populations as well as in the formation of bloom populations are considered, and recommendations for future research are presented.

Similarities between the biochemical composition of jellyfish body and mucus.

Recognition of the importance of jellyfish in marine ecosystems is growing. Yet, the biochemical composition of the mucus that jellyfish constantly excrete is poorly characterized. Here we analyzed the macromolecular (proteins, lipids and carbohydrates) and elemental (carbon and nitrogen) composition of the body and mucus of five scyphozoan jellyfish species (Aurelia aurita, Chrysaora fulgida, Chrysaora pacifica, Eupilema inexpectata and Rhizostoma pulmo). We found that the relative contribution of the different macromolecules and elements in the jellyfish body and mucus was similar across all species, with protein being the major component in all samples (81 ± 4% of macromolecules; 3.6 ± 3.1% of dry weight, DW) followed by lipids (13 ± 4% of macromolecules; 0.5 ± 0.4%DW) and carbohydrates (6 ± 3% of macromolecules; 0.3 ± 0.4%DW). The energy content of the jellyfish matter ranged from 0.2 to 3.1 KJ g-1 DW. Carbon and nitrogen content was 3.7 ± 3.0 and 1.0 ± 0.8%DW, respectively. The average ratios of protein:lipid:carbohydrate and carbon:nitrogen for all samples were 14.6:2.3:1 and 3.8:1, respectively. Our study highlights the biochemical similarity between the jellyfish body and mucus and provides convenient and valuable ratios to support the integration of jellyfish into trophic and biogeochemical models.

Extreme changes in salinity drive population dynamics of Catostylus mosaicus medusae in a modified estuary.

Modifications to estuaries through the construction of barrages alter the natural dynamics of inhabitant species by controlling freshwater inputs into those systems. To understand the effects of modified freshwater flows on a native scyphozoan jellyfish, Catostylus mosaicus, and to identify the environmental drivers of medusa occurrence, we analysed a 20-year observational dataset composed of 11 environmental variables and medusa presence/absence from 15 sampling stations located below the Fitzroy Barrage, in the Fitzroy River, Queensland. Major decreases in salinity (minimum salinity 0) occurred approximately 16 times during the 20-year period and medusae disappeared from the estuary following every major freshwater flow event. Salinity was identified as the most influential variable contributing to variation in the number of upper estuary sites reporting jellyfish. We then ran two laboratory experiments to test the following hypotheses: (i) prolonged decreases in salinity impair survival, pulsation, and respiration rates of C. mosaicus medusae; and (ii) transient decreases temporarily impair pulsation and respiration but medusae recover when salinity returns to normal levels. Medusae were unable to survive extended periods at extreme low salinities, such that they would experience when a barrage opens fully, but had significantly higher survival and recovery rates following smaller, transient changes to salinity that might occur following a moderate rainfall event. This demonstrates for the first time that modification of freshwater flow by a barrage regulates the population dynamics of an estuarine jellyfish, and highlights the need for robust, long term datasets, and to firmly embed experimental approaches in realistic ecological contexts.

Habitat partitioning in Antarctic krill: Spawning hotspots and nursery areas.

Antarctic krill, Euphausia superba, have a circumpolar distribution but are concentrated within the south-west Atlantic sector, where they support a unique food web and a commercial fishery. Within this sector, our first goal was to produce quantitative distribution maps of all six ontogenetic life stages of krill (eggs, nauplii plus metanauplii, calyptopes, furcilia, juveniles, and adults), based on a compilation of all available post 1970s data. Using these maps, we then examined firstly whether "hotspots" of egg production and early stage nursery occurred, and secondly whether the available habitat was partitioned between the successive life stages during the austral summer and autumn, when krill densities can be high. To address these questions, we compiled larval krill density records and extracted data spanning 41 years (1976-2016) from the existing KRILLBASE-abundance and KRILLBASE-length-frequency databases. Although adult males and females of spawning age were widely distributed, the distribution of eggs, nauplii and metanauplii indicates that spawning is most intense over the shelf and shelf slope. This contrasts with the distributions of calyptope and furcilia larvae, which were concentrated further offshore, mainly in the Southern Scotia Sea. Juveniles, however, were strongly concentrated over shelves along the Scotia Arc. Simple environmental analyses based on water depth and mean water temperature suggest that krill associate with different habitats over the course of their life cycle. From the early to late part of the austral season, juvenile distribution moves from ocean to shelf, opposite in direction to that for adults. Such habitat partitioning may reduce intraspecific competition for food, which has been suggested to occur when densities are exceptionally high during years of strong recruitment. It also prevents any potential cannibalism by adults on younger stages. Understanding the location of krill spawning and juvenile development in relation to potentially overlapping fishing activities is needed to protect the health of the south-west Atlantic sector ecosystem.

Environmental control of asexual reproduction and somatic growth of Aurelia spp. (Cnidaria, Scyphozoa) polyps from the Adriatic Sea.

Polyps of two moon jellyfish species, Aurelia coerulea and A. relicta, from two Adriatic Sea coastal habitats were incubated under multiple combinations of temperature (14, 21°C), salinity (24, 37 ppt) and food regime (9.3, 18.6, 27.9 µg C ind-1 week-1) to comparatively assess how these factors may influence major asexual reproduction processes in the two species. Both species exhibited a shared pattern of budding mode (Directly Budded Polyps: DBP; Stolonal Budded Polyps: SBP), with DBP favoured under low food supply (9.3 µg C ind -1 week-1) and low temperature (14°C), and SBP dominant under high temperature (21°C). However, A. coerulea showed an overall higher productivity than A. relicta, in terms of budding and podocyst production rates. Further, A. coerulea exhibited a wide physiological plasticity across different temperatures and salinities as typical adaptation to ecological features of transitional coastal habitats. This may support the hypothesis that the invasion of A. coerulea across coastal habitats worldwide has been driven by shellfish aquaculture, with scyphistoma polyps and resting stages commonly found on bivalve shells. On the contrary, A. relicta appears to be strongly stenovalent, with cold, marine environmental optimal preferences (salinity 37 ppt, T ranging 14-19°C), corroborating the hypothesis of endemicity within the highly peculiar habitat of the Mljet lake. By exposing A. relicta polyps to slightly higher temperature (21°C), a previously unknown developmental mode was observed, by the sessile polyp regressing into a dispersive, temporarily unattached and tentacle-less, non-feeding stage. This may allow A. relicta polyps to escape climatic anomalies associated to warming of surface layers and deepening of isotherms, by moving into deeper, colder layers. Overall, investigations on species-specific eco-physiological and ontogenetic potentials of polyp stages may contribute to clarify the biogeographic distribution of jellyfish and the phylogenetic relationships among evolutionary related sister clades.

Occurrence of the siphonophore Muggiaea atlantica in Scottish coastal waters: source or sink?

We applied the concept of source-sink dynamics to investigate a recent (1999-2013) increase in the occurrence of the siphonophore Muggiaea atlantica in Scottish coastal waters. Our aim was to determine whether this change represented the establishment of resident populations (i.e. "sources"), or transient populations reliant on immigration (i.e. "sinks"). First, we show that local production was not always sufficient to account for recruitment (a "source" prerequisite), suggesting reliance on immigration (a "sink" prerequisite). Using variation partitioning, we then discriminated between the exclusive effects of immigration [indexed by the European Slope Current (ESC)] and local production (indexed by local sea temperature and food availability). On the west coast (Loch Ewe), interannual variability in the species' abundance was determined by, in order of increasing importance: (i) suitable local environmental conditions (13%); (ii) the role of the ESC in modulating these conditions (20%); and (iii) immigration via the ESC (29%). These results provided a strong indication that Loch Ewe represents a sink habitat for M. atlantica. However, on the east coast (Stonehaven) our results were less conclusive, probably due to the less direct influence of the ESC. For both locations, we suggest that low winter temperatures prevented overwintering, necessitating annual re-colonization via immigration.

Respiratory response to temperature of three populations of Aurelia aurita polyps in northern Europe.

The benthic life stage (polyp or scyphistoma) of the bloom-forming jellyfish, Aurelia aurita (Linnaeus, 1759), also known as the moon jellyfish, contributes to the seasonal occurrence and abundance of medusa blooms via asexual reproduction. A. aurita is widely distributed in coastal areas in northern Europe, and one of the most studied jellyfish species. While the physiology of the visible medusa is largely understood, understanding of the physiology of the perennial benthic life-stage is scarce. To measure the physiological tolerance of A. aurita, the scyphistoma's temperature sensitivity across its distributional range was investigated. Respiration rates of polyps from three northern European locations exposed to 11 temperatures between 2 and 22°C were measured. There was a significant difference in respiration rate among the three polyp populations, which may reflect on differences in their thermal tolerance window. A critical temperature was reached at 14°C with the metabolic rate decreasing below and above that temperature. This pattern was less pronounced in the Norwegian population but polyps were able to survive, at least temporarily, those temperatures exceeding their natural range. While polyps collected from northern Norway, with a narrow environmental thermal window, displayed a low baseline metabolism with a Q10 value of 1.2, polyps from southern England and Scotland had Q10 values of 1.6 and 2.5, respectively. Differences in polyps' respiration rates across their distributional range suggest that populations have evolved adaptations to local environmental thermal conditions.

Female and male gamete mitochondria are distinct and complementary in transcription, structure, and genome function.

Respiratory electron transport in mitochondria is coupled to ATP synthesis while generating mutagenic oxygen free radicals. Mitochondrial DNA mutation then accumulates with age, and may set a limit to the lifespan of individual, multicellular organisms. Why is this mutation not inherited? Here we demonstrate that female gametes-oocytes-have unusually small and simple mitochondria that are suppressed for DNA transcription, electron transport, and free radical production. By contrast, male gametes-sperm-and somatic cells of both sexes transcribe mitochondrial genes for respiratory electron carriers and produce oxygen free radicals. This germ-line division between mitochondria of sperm and egg is observed in both the vinegar fruitfly and the zebrafish-species spanning a major evolutionary divide within the animal kingdom. We interpret these findings as an evidence that oocyte mitochondria serve primarily as genetic templates, giving rise, irreversibly and in each new generation, to the familiar energy-transducing mitochondria of somatic cells and male gametes. Suppressed mitochondrial metabolism in the female germ line may therefore constitute a mechanism for increasing the fidelity of mitochondrial DNA inheritance.

Energy, ageing, fidelity and sex: oocyte mitochondrial DNA as a protected genetic template.

Oxidative phosphorylation couples ATP synthesis to respiratory electron transport. In eukaryotes, this coupling occurs in mitochondria, which carry DNA. Respiratory electron transport in the presence of molecular oxygen generates free radicals, reactive oxygen species (ROS), which are mutagenic. In animals, mutational damage to mitochondrial DNA therefore accumulates within the lifespan of the individual. Fertilization generally requires motility of one gamete, and motility requires ATP. It has been proposed that oxidative phosphorylation is nevertheless absent in the special case of quiescent, template mitochondria, that these remain sequestered in oocytes and female germ lines and that oocyte mitochondrial DNA is thus protected from damage, but evidence to support that view has hitherto been lacking. Here we show that female gametes of Aurelia aurita, the common jellyfish, do not transcribe mitochondrial DNA, lack electron transport, and produce no free radicals. In contrast, male gametes actively transcribe mitochondrial genes for respiratory chain components and produce ROS. Electron microscopy shows that this functional division of labour between sperm and egg is accompanied by contrasting mitochondrial morphology. We suggest that mitochondrial anisogamy underlies division of any animal species into two sexes with complementary roles in sexual reproduction. We predict that quiescent oocyte mitochondria contain DNA as an unexpressed template that avoids mutational accumulation by being transmitted through the female germ line. The active descendants of oocyte mitochondria perform oxidative phosphorylation in somatic cells and in male gametes of each new generation, and the mutations that they accumulated are not inherited. We propose that the avoidance of ROS-dependent mutation is the evolutionary pressure underlying maternal mitochondrial inheritance and the developmental origin of the female germ line.

Jellyfish body plans provide allometric advantages beyond low carbon content.

Jellyfish form spectacular blooms throughout the world's oceans. Jellyfish body plans are characterised by high water and low carbon contents which enables them to grow much larger than non-gelatinous animals of equivalent carbon content and to deviate from non-gelatinous pelagic animals when incorporated into allometric relationships. Jellyfish have, however, been argued to conform to allometric relationships when carbon content is used as the metric for comparison. Here we test the hypothesis that differences in allometric relationships for several key functional parameters remain for jellyfish even after their body sizes are scaled to their carbon content. Data on carbon and nitrogen contents, rates of respiration, excretion, growth, longevity and swimming velocity of jellyfish and other pelagic animals were assembled. Allometric relationships between each variable and the equivalent spherical diameters of jellyfish and other pelagic animals were compared before and after sizes of jellyfish were standardised for their carbon content. Before standardisation, the slopes of the allometric relationships for respiration, excretion and growth were the same for jellyfish and other pelagic taxa but the intercepts differed. After standardisation, slopes and intercepts for respiration were similar but excretion rates of jellyfish were 10× slower, and growth rates 2× faster than those of other pelagic animals. Longevity of jellyfish was independent of size. The slope of the allometric relationship of swimming velocity of jellyfish differed from that of other pelagic animals but because they are larger jellyfish operate at Reynolds numbers approximately 10× greater than those of other pelagic animals of comparable carbon content. We conclude that low carbon and high water contents alone do not explain the differences in the intercepts or slopes of the allometric relationships of jellyfish and other pelagic animals and that the evolutionary longevity of jellyfish and their propensity to form blooms is facilitated by their unique body plans.