Juvenile Medusae Research Articles

CO2‐induced seawater acidification impairs the stinging cells of a jellyfish

AbstractCO2‐induced seawater acidification has been shown to modify predator–prey interactions in many marine taxa. Scyphozoans play an important role in the trophic dynamics of marine ecosystems during their blooms in coastal waters; however, the impacts of seawater acidification on the predation behavior of these animals are poorly understood. Here, we aimed to examine the impact of a decrease in seawater pH on the feeding behavior and growth of ephyrae (juvenile medusae) of the scyphozoan Aurelia coerulea. Combining bulk and single‐cell RNA sequencing approaches, we assessed transcriptomic changes of ephyrae under a laboratory‐based pH 7.6 condition. We found that the feeding rates and growth of ephyrae were significantly inhibited by a decrease in seawater pH. Furthermore, transcriptome analysis showed that a decline in pH significantly reduced the expression of genes related to toxins and nematocyst structure in ephyrae. These findings were further confirmed by single‐cell transcriptomic analyses and revealed that low pH impaired the toxin activity and energy metabolism of stinging cells. The pH recovery experiment indicated that moving ephyrae from seawater with pH 7.6 into seawater with pH 8.1 greatly restored their feeding, growth, and toxin‐related and nematocyst structure–related gene expression. However, exposure to pH 7.6 for 23 d could not recover the decrease in the feeding and growth of ephyrae. Together, these findings indicate that CO2‐induced acidification compromised the stinging cells of A. coerulea ephyrae, with concomitant negative consequences on predation and growth that are likely to alter predator–prey interactions, with consequent effects on community structure and ecosystem.

Correlative Light, Electron Microscopy and Raman Spectroscopy Workflow To Detect and Observe Microplastic Interactions with Whole Jellyfish.

Many researchers have turned their attention to understanding microplastic interaction with marine fauna. Efforts are being made to monitor exposure pathways and concentrations and to assess the impact such interactions may have. To answer these questions, it is important to select appropriate experimental parameters and analytical protocols. This study focuses on medusae of Cassiopea andromeda jellyfish: a unique benthic jellyfish known to favor (sub-)tropical coastal regions which are potentially exposed to plastic waste from land-based sources. Juvenile medusae were exposed to fluorescent poly(ethylene terephthalate) and polypropylene microplastics (<300 μm), resin embedded, and sectioned before analysis with confocal laser scanning microscopy as well as transmission electron microscopy and Raman spectroscopy. Results show that the fluorescent microplastics were stable enough to be detected with the optimized analytical protocol presented and that their observed interaction with medusae occurs in a manner which is likely driven by the microplastic properties (e.g., density and hydrophobicity).

Ingestion, egestion and physiological effects of polystyrene microplastics on the marine jellyfish Rhopilema esculentum

Jellyfish are planktonic predators that may be susceptible to ingesting microplastics. However, the effects of MP exposure on jellyfish are poorly understood. In this study, the ingestion and egestion of polystyrene microbeads, and its chronic physiological effects on Rhopilema esculentum at an environmental concentration (100 items/L) and a predicted concentration (1000 items/L) were evaluated. The results showed that the ingestion amount of juvenile medusae was relatively low. The MP egestion rates reached 100 % within 9 h of clearance. Chronic exposure (15 days) to MPs at environmental concentrations led to no adverse impacts. Nevertheless, the predicted concentration of MP exposure induced growth inhibition, a reduction in assimilation efficiency, oxygen consumption increase, and lipase enzyme activity reduction in the jellyfish, indicating that MPs can cause adverse effects on the energy budget of jellyfish in the near future. Our study provides new insights into the potential risk of MPs in marine environments.

Multiple reproduction forms in the polyps of the cannonball jellyfish Stomolophus sp. 2: Probable life-cycle reversal.

The jellyfish genera Stomolophus spp. is one of the most abundant in the Pacific Ocean, yet it has not been thoroughly studied. Until recently, research has been developed and directed to its knowledge because of the economic interest in its exploitation. The genus Stomolophus in the Pacific Ocean is composed of five species (S. agaricus,S. chunii, S. collaris, S. fritillaria,and S. meleagris), and Stomolophus sp. 2 has been recently reported in the central part of the Gulf of California. Therefore, this study aimed to describe in vivo the different developmental stages of Stomolophus sp. 2 life cycle. As a result, multiple polyp reproduction forms were described, such as polyp-stolon formation, polydisc strobilation with more than 20 ephyrae formed by each strobila, and polyp formation directly from juvenile ephyra. In the degenerating phase, the polyps turned into cysts induced by stress conditions, such as changes in temperature, oxygen, and food availability. The life cycle of Stomolophus sp. 2 can be distinguished from that of S. meleagris by showing various asexual reproduction mechanisms and polydisc-like strobilation. The formation of polyps directly from the ectoderm of degenerating juvenile medusae suggests the possibility of a reversion cycle. Because of the different life cycles between S. meleagris and S. sp. 2, in addition to their morphological and genetic differences, this study proposes that Stomolophus sp. 2 should be considered a new species and suggests the name Stomolophus yaquilli, in reference to the indigenous community that lives in the species distribution area.

Evaluation of digestive capacity in the polyp, ephyrae, and medusae stages of the cannonball jellyfish Stomolophus meleagris

The digestive capacity of jellyfish has barely been studied because of the complexity of their life stage body-forms and sizes. To assess the digestive capacity in the changes from the benthic polyp-form to the pelagic stage in the cannonball jellyfish Stomolophus meleagris, we used fluorometric and spectrophotometric techniques for measuring the activity of trypsin, chymotrypsin, aminopeptidase, amylase, lipase, phosphatase acid, and alkaline. The findings showed that at all stages were able to digest proteins, carbohydrates, and lipids, but the digestive capacity differs between the benthic–pelagic stage and final development of the ephyrae, suggesting a shift in nutrient requirements. The digestive capacity indicated that polyps better assimilate carbohydrates and proteins. During the pelagic stage, a shift in the digestive capacity occurred, where 5-day ephyrae better assimilate proteins, while 15-day-old ephyrae were better with lipids and proteins and juvenile medusae with lipids. This is the first study to describe changes in the digestive capacity of cannonball jellyfish and can help identify ecological features of an important fishing resource with potential aquaculture interest. Different diets for polyps, ephyrae, and juvenile medusae must be considered if the species is cultivated.

Transcriptome analysis of scyphozoan jellyfish Rhopilema esculentum from polyp to medusa identifies potential genes regulating strobilation.

Strobilation is a unique asexual reproduction mode of scyphozoan jellyfish, through which benthic polyp develops into pelagic medusa. It is an orderly metamorphosis process triggered by environmental signals. However, the knowledges of molecular mechanisms under the drastic morphological and physiological changes are still limited. In this study, the transcriptomes from polyps to juvenile medusae at different stages were characterized by RNA-seq in scyphozoan jellyfish Rhopilema esculentum. Among 96,076 de novo assembled unigenes, 7090 differentially expressed genes (DEGs) were identified during the developmental stages. The co-expression pattern analysis of DEGs yielded 15 clusters with different expression patterns. Among them, a cluster with 388 unigenes was related to strobila. In this specific cluster, the GO terms related to "sequence-specific DNA binding transcription factor activity" and "sequence-specific DNA binding" were significantly enriched. Transcription factors, including segmentation protein even-skipped-like, segmentation polarity protein engrailed-like, homeobox proteins Otx-like, Twist-like and Cnox2-Pc-like, as well as genes such as RxR-like and Dmrtf-like, were identified to be potentially involved in strobilation. Their expression patterns and the other 11 TFs/genes involved in strobilation were confirmed with qRT-PCR methods. The present study pointed out the role of transcription factors in strobilation and produced a list of novel candidate genes for further studies. It could provide valuable information for understanding the molecular mechanisms of jellyfish strobilation.

Life Cycle Reversal in Aurelia sp.1 (Cnidaria, Scyphozoa).

The genus Aurelia is one of the major contributors to jellyfish blooms in coastal waters, possibly due in part to hydroclimatic and anthropogenic causes, as well as their highly adaptive reproductive traits. Despite the wide plasticity of cnidarian life cycles, especially those recognized in certain Hydroza species, the known modifications of Aurelia life history were mostly restricted to its polyp stage. In this study, we document the formation of polyps directly from the ectoderm of degenerating juvenile medusae, cell masses from medusa tissue fragments, and subumbrella of living medusae. This is the first evidence for back-transformation of sexually mature medusae into polyps in Aurelia sp.1. The resulting reconstruction of the schematic life cycle of Aurelia reveals the underestimated potential of life cycle reversal in scyphozoan medusae, with possible implications for biological and ecological studies.

The case ofBougainvillia triestinaHartlaub 1911 (Hydrozoa, Cnidaria): a 100-year-long struggle for recognition

Bougainvillia triestina was described by Hartlaub in 1911 from specimens collected in the Gulf of Trieste (North Adriatic, Italy). Two years later, after re-examination of the same specimens, Neppi & Stiasny (1913) concluded that these were in fact juvenile medusae of Bougainvillia autumnalis (now synonymized with Bougainvillia muscus). Based on unique morphological traits and genetic analyses (16S rRNA, 18S rRNA, COI) of specimens of different stages recently collected in the shallow and enclosed coastal area of Ploce Harbour and Mali Ston Bay (South Adriatic, Croatia), we can confirm, 100 years after its first description, B. triestina as a valid, distinct species, clearly distinguishable from B. muscus (Allman 1863). Based on its occurrence in the Adriatic Sea, B. triestina seems to prefer productive coastal areas with a wide range of temperatures and salinities. Therefore, we expect that this species inhabits other coastal areas of the Mediterranean Sea as well as those of other seas and oceans. Given this, it is probable that in previous investigations some records of B. triestina were incorrectly attributed to B. muscus.

Comparative muscle development of scyphozoan jellyfish with simple and complex life cycles.

BackgroundSimple life cycles arise from complex life cycles when one or more developmental stages are lost. This raises a fundamental question - how can an intermediate stage, such as a larva, be removed, and development still produce a normal adult? To address this question, we examined the development in several species of pelagiid jellyfish. Most members of Pelagiidae have a complex life cycle with a sessile polyp that gives rise to ephyrae (juvenile medusae); but one species within Pelagiidae, Pelagia noctiluca, spends its whole life in the water column, developing from a larva directly into an ephyra. In many complex life cycles, adult features develop from cell populations that remain quiescent in larvae, and this is known as life cycle compartmentalization and may facilitate the evolution of direct life cycles. A second type of metamorphic processes, known as remodeling, occurs when adult features are formed through modification of already differentiated larval structures. We examined muscle morphology to determine which of these alternatives may be present in Pelagiidae.ResultsWe first examined the structure and development of polyp and ephyra musculature in Chrysaora quinquecirrha, a close relative of P. noctiluca with a complex life cycle. Using phallotoxin staining and confocal microscopy, we verified that polyps have four to six cord muscles that persist in strobilae and discovered that cord muscles is physically separated from ephyra muscle. When cord muscle is removed from ephyra segments, normal ephyra muscle still develops. This suggests that polyp cord muscle is not necessary for ephyra muscle formation. We also found no evidence of polyp-like muscle in P. noctiluca. In both species, we discovered that ephyra muscle arises de novo in a similar manner, regardless of the life cycle.ConclusionsThe separate origins of polyp and ephyra muscle in C. quinquecirrha and the absence of polyp-like muscle in P. noctiluca suggest that polyp muscle is not remodeled to form ephyra muscle in Pelagiidae. Life cycle stages in Scyphozoa may instead be compartmentalized. Because polyp muscle is not directly remodeled, this may have facilitated the loss of the polyp stage in the evolution of P. noctiluca.Electronic supplementary materialThe online version of this article (doi:10.1186/s13227-015-0005-7) contains supplementary material, which is available to authorized users.

Prey concentration and temperature effect on budding and strobilation of Aurelia sp. 1 polyps

Aurelia spp. are among the main blooming jellyfish species. The polyp stage plays an important role in its outbreaks. To determine how temperature and food conditions may affect the process of reproduction, we maintained Aurelia sp. 1 polyps in the laboratory at three temperatures (10–15°C) and four food concentrations (0–0.1 mg C l−1) to test their combined effects on the strobilation process and the production of buds and ephyrae. The length of the strobilation preparation period significantly decreased with increased temperature, but was not affected by food conditions. With sufficient food supply, the polyps that had already released ephyrae restart the strobilation process. Food condition positively affects both the production of buds and ephyrae. Temperature, however, had different effects: at the three temperatures tested, 13°C was most appropriate for polyps to release ephyrae, while bud production was highest at 15°C. These results suggest that eutrophication (as a proxy for food condition) would affect both the size of the Aurelia sp. 1 polyp population and juvenile medusa population, whereas temperature adjusts the reproductive energy distribution between budding and ephyra release to regulate the strobilation process. This temperature adjustment mechanism likely helps match the production of juvenile medusae with the peak of zooplankton biomass.

Cell proliferation in cubozoan jellyfish Tripedalia cystophora and Alatina moseri.

Cubozoans (box jellyfish) undergo remarkable body reorganization throughout their life cycle when, first, they metamorphose from swimming larvae to sessile polyps, and second, through the metamorphosis from sessile polyps to free swimming medusae. In the latter they develop complex structures like the central nervous system (CNS) and visual organs. In the present study several aspects of cell proliferation at different stages of the life cycle of the box jellyfish Tripedalia cystophora and Alatina moseri have been examined through in vivo labeling of cells in the synthetic phase (S phase) of the cell cycle. Proliferation zones were found in metamorphosing polyps, as well as in juvenile medusae, where both the rhopalia and pedalia have enhanced rates of proliferation. The results also indicate a rather fast cell turnover in the rhopalia including the rhopalial nervous system (RNS). Moreover, T. cystophora showed diurnal pattern of cell proliferation in certain body parts of the medusa, with higher proliferation rates at nighttime. This is true for two areas in close connection with the CNS: the stalk base and the rhopalia.

The hydroid and early medusa stage ofOlindias formosus(Cnidaria, Hydrozoa, Limnomedusae)

Olindiasspp. medusae are found worldwide in sublittoral tropical and sub-tropical coastal regions; their occurrence near shore can result in human envenomation events. While behaviour of medusae and human contact with medusae has been documented for the genus, the hydroid (polyp) phase of theOlindiaslife cycle has eluded investigators for over a century. Given the recent debate among public media and scientific communities that jellyfish blooms are increasing worldwide, there is a growing urgency to understand how and why jellyfish populations bloom. In order to understand jellyfish population dynamics, the asexual benthic phase must be studied to determine when, where, and how juvenile medusae are produced. In this study, husbandry management strategies, including the creation of artificial habitat forOlindias formosusmedusae in aquaria were developed to encourage spawning and larval settlement. The resultant hydroid colony ofOlindias formosuswas discovered in November of 2012, utilizing the natural fluorescence of the medusa as a detection method. A description of the hydroid and early medusa stage is presented. These techniques provide a basis for locatingin situthe benthic hydroid phases within this genus and other fluorescent medusae, the discovery of which may lead to a better understanding of the causative factors for jellyfish blooms.

Embryos, polyps and medusae of the Early Cambrian scyphozoan Olivooides

The Early Cambrian organism Olivooides is known from both embryonic and post-embryonic stages and, consequently, it has the potential to yield vital insights into developmental evolution at the time that animal body plans were established. However, this potential can only be realized if the phylogenetic relationships of Olivooides can be constrained. The affinities of Olivooides have proved controversial because of the lack of knowledge of the internal anatomy and the limited range of developmental stages known. Here, we describe rare embryonic specimens in which internal anatomical features are preserved. We also present a fuller sequence of fossilized developmental stages of Olivooides, including associated specimens that we interpret as budding ephyrae (juvenile medusae), all of which display a clear pentaradial symmetry. Within the framework of a cnidarian interpretation, the new data serve to pinpoint the phylogenetic position of Olivooides to the scyphozoan stem group. Hypotheses about scalidophoran or echinoderm affinities of Olivooides can be rejected.

Growth, Development and Temporal Variation in the Onset of Six Chironex fleckeri Medusae Seasons: A Contribution to Understanding Jellyfish Ecology

Despite the worldwide distribution, toxicity and commercial, industrial and medical impacts jellyfish present, many aspects of their ecology remain poorly understood. Quantified here are important ecological parameters of Chironex fleckeri medusae, contributing not only to the understanding of an understudied taxon, the cubozoa, but also to the broader understanding of jellyfish ecology. C. fleckeri medusae were collected across seven seasons (1999, 2000, 2003, 2005–07 and 2010), with growth rates, temporal variation in the medusae season onset and differences in population structure between estuarine and coastal habitats quantified. With a mean of 2 September ±2 d (mean ±95% confidence limits), the earliest date of metamorphosis was temporally constrained between seasons, varying by only 7 d (30 August to 5 September). Juvenile medusae appeared to be added over an extended period, suggesting polyp metamorphosis was an ongoing process once it commenced. At a maximum of 3±0.2 mm d−1 IPD, medusae growth to an asymptotic size of ∼190 mm IPD was rapid, yet, with the oldest medusae estimated to be ∼78 d in age, medusae did not appear to accumulate along the coastline. Furthermore, a greater proportion of juveniles were observed along the coastline, with estuarine populations typified by larger medusae. With key aspects of C. fleckeri's ecology now quantified, medusae season management protocols can be further developed.

Anomalous Infrared Taxis of an Aquatic Animal, the Giant Jellyfish Nemopilema nomurai (Scyphozoa, Rhizostomeae)

Remote sensing of thermal radiation (infrared wavelengths) has been reported only in some terrestrial animals and is known to have significant physiological and ecological meaning. In aquatic animals, however, it has not even been discussed because water almost completely absorbs infrared (IR) wavelengths, and such sensitivity has been regarded as useless in aquatic environments. Here we report, for the first time, an anomalous behavior—swimming toward an IR-radiating source—in an aquatic animal, the giant jellyfish, Nemopilema nomurai. Experiments were performed with laboratory-reared juvenile medusae of Nemopilema in a small experimental chamber. In all 52 trials, the majority (average: 78.3%; variation: 63.3%– 94.3%) of the medusae gathered on the IR-irradiated half of the chamber. Near-IR (850/940 nm) and visible light neither attracted the medusae nor induced taxis. A series of results indicated that the juveniles of Nemopilema tended to flock toward a mass of warmer water. Although the exact physiological and ecological meaning of this behavior is uncertain, it might be possible to consider infrared taxis as one of the behaviors in marine ecosystems. It may thus be useful to re-examine the swarming behavior reported in some jellyfish species from the viewpoint of IR taxis. Infrared (IR) sensitivity is known to be mediated by the so-called pit organs, which enable crotaline and boid snakes to apprehend homeothermic prey (1–7) and vampire bats to detect IR radiation from blood-rich locations (8, 9). Moreover, similar mechanisms have been reported in some insects such as fine debris species of beetle (10–13), bloodsucking bugs (14), and some butterflies (15, 16). In aquatic animals, however, little is known about the IR sensitivity. This is the first report to describe an anomalous IR-tactic behavior in the giant jellyfish, Nemopilema nomurai, living in an aquatic environment. Nemopilema nomurai Kishinouye 1922 is one of the largest scyphozoan jellyfish, measuring 1–2 m in diameter and weighing 100–200 kg. Massive blooms of this species have occurred almost annually since 2002, severely affecting coastal fisheries in the Sea of Japan. The life cycle of N. nomurai has been well established by us and our coworkers (17, 18), so the juvenile medusae are easily available. We thus used laboratory-reared juveniles (extended bell diameter, 8–15 mm) to examine the IR sensitivity of N. nomurai. The experimental chamber (width 30 cm, length 24 cm, height 16 cm) used to test IR sensitivity was made from transparent acryl resin plate (5 mm thick). It was filled with seawater to a depth of 3.5 cm and 20 to 35 juvenile individuals were added. The distribution of the medusae in the chamber was monitored by photographing them from above with a photographic strobe every 30 or 60 min. The IR wavelengths were obtained from a tungsten-filament lamp (40 W) by passing the light through a long-pass filter (50% cut-on at 990 nm; LIO-990, Asahi Spectra Co. Ltd.). The tungsten-filament lamp was fixed in a lightproof aluminum housing with a window, where the long-pass filter was mounted. All possible heat sources, except for the IR-wavelength source, were excluded from around the experimental chamber. Near-IR wavelengths, 940 and 850 nm, were obtained from two types of 1.2-W LEDs, LB12WP01 and LC12-WP01 (Ebisu Electronics Co. Ltd.), reReceived 1 August 2011; accepted 20 October 2011. * To whom correspondence should be addressed. E-mail: ohtsu@ life.shimane-u.ac.jp Reference: Biol. Bull. 221: 243–247. (December 2011) © 2011 Marine Biological Laboratory

Ontogenetic Changes in the Bell Morphology and Kinematics and Swimming Behavior of Rowing Medusae: the Special Case of the Limnomedusa Liriope tetraphylla

Swimming animals may experience significant changes in the Reynolds number (Re) of their surrounding fluid flows throughout ontogeny. Many medusae experience Re environments with significant viscous forces as small juveniles but inertially dominated Re environments as adults. These different environments may affect their propulsive strategies. In particular, rowing, a propulsive strategy with ecological advantages for large adults, may be constrained by viscosity for small juvenile medusae. We examined changes in the bell morphology and swimming kinematics of the limnomedusa Liriope tetraphylla at different stages of development. L. tetraphylla maintained an oblate bell (fineness ratio ≈ 0.5-0.6), large velar aperture ratio (R(v) ≈ 0.5-0.8), and rapid bell kinematics throughout development. These traits enabled it to use rowing propulsion at all stages except the very smallest sizes observed (diameter = 0.14 cm). During the juvenile stage, very rapid bell kinematics served to increase Re sufficiently for rowing propulsion. Other taxa that use rowing propulsion as adults, such as leptomedusae and scyphomedusae, typically utilize different propulsive strategies as small juveniles to function in low Re environments. We compared the performance values of the different propulsive modes observed among juvenile medusae.

Documentation of potential courtship-behaviour in Periphylla periphylla (Cnidaria: Scyphozoa)

The distribution pattern and nocturnal surface behaviour of the deep-sea medusa Periphylla periphylla in a Norwegian fjord was studied. Medusa abundance, size distribution and condition were determined, using surface collections, net tows and ROV-based video profiles. Only larger, mature medusae reached the surface and aggregated into small groups of both sexes, whereas juvenile medusae remained in deeper waters. Observations on the behaviour and cytology of aggregated medusae suggested a mating strategy. We hypothesize that this behaviour is the by-product of a holopelagic life history, developed in a more oceanic deep environment with low species abundance, as surface aggregation increases the chance of encounter and mating.

Reproduction and longevity of Aurelia labiata in Roscoe Bay, a small bay on the Pacific coast of Canada

Reproduction by the moon jelly, Aurelia labiata, was observed in a small bay on the west coast of Canada. The bay is located in an area isolated from human contact except in the summer, is sheltered from wind and wave action by mountain ridges, and has limited tidal flushing due to a gravel bar at the entrance that dries at lower low water. Planulae appeared in brood sacs beginning in October and November. The planulae were shed by the end of March and ephyrae emerged in June. Juvenile medusae were estimated to constitute about 30—40% of medusae in the bay in each of the two years of this study. Medusae remained in the bay throughout the year. There was no major visible mortality in the adult population during the two year observation period. Medusae appear to be lost from the bay as a result of tidal flushing. It is argued that in Roscoe Bay Aurelia labiata medusae live for more than one year and that up to 40% of the adult medusae may be two years of age or older.

New observations and corrections concerning the trio of invasive hydromedusae &lt;i&gt;Maeotias marginata (=M. inexpectata), Blackfordia virginica&lt;/i&gt;, and &lt;i&gt;Moreisia&lt;/i&gt; sp. in the San Francisco Estuary

New observations of Maeotias, Blackfordia, and Moerisia in low salinity waters of the San Francisco Bay estuary allow better understanding of the life cycles and natural history of these three genera of invading hydrozoans. Maeotias inexpectata Ostroumoff, 1896 is found to be a junior synonym of Maeotias marginata (Modeer, 1791). Moreover, M. inexspectata Ostroumoff, 1896b is an incorrect subsequent spelling of M. inexpectata Ostroumoff, 1896a. The clear presence of marginal statocysts in the medusa of this species places it back in the family Olindiidae of the Limnomedusae. Polyps previously attributed to Maeotias in San Francisco Bay are now known to belong to a Moerisia sp., whose medusa has also recently been found in the estuary system. Solitary Moerisia polyps have been found in the field amongst the general fouling fauna on floating docks in the Napa River. Small simple primary polyps of M. marginata were obtained in the laboratory. Polyps of Blackfordia virginica have been found in abundance in the field covering the valves of nonindigenous barnacles in the Napa River and laboratory-cultured colonies are pictured here along with their newly-released and juvenile medusae.