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Cassiopea and Its Zooxanthellae
Abstract
As many cnidarians, the upside-down jellyfish Cassiopea spec. lives in an obligate symbiosis with its zooxanthellae: Dinoflagellates of the genus Symbiodinium. The symbiosis seems mutual and both partners have adapted to suit the partner’s needs. Despite the very close co-operation the zooxanthellae are not transmitted vertically but are taken up from the water column during the polyp stage. Polyps seem flexible which clades to internalize and usually take up all clades available but medusae seem much more restrictive and as far as we know only co-operate with a single Symbiodinium clade (the clade however can vary between individuals). The Cassiopea-symbiont interaction is especially interesting for researchers as Cassiopea occurs in shallow lagoon waters meaning a quite stressful environment with high temperatures and high levels of irradiation as well as potentially drastic changes in salinity and sedimentation rates. In other cnidarian-zooxanthellae partnerships these conditions would lead to a severe disturbance of the symbiosis often ultimately leading to the death of the holobiont (bleaching). The Cassiopea/Symbiodinium interaction, however, is an example of a successful co-operation under stressful environmental conditions and therefore interesting also in the context of climate change. This chapter summarizes our knowledge of the symbiosis of Cassiopea and its zooxanthellae focusing on uptake and choice of symbiosis partners by Cassiopea as well as the adaptations making the co-operation possible.
... Cassiopea, a genus of symbiotic jellyfish (Schyphozoa, Rhizostomae), is an emerging model organism for the study of cnidarian-algal symbiosis [30][31][32]. Similar to corals, Cassiopea is associated with dinoflagellates of the family Symbiodiniaceae. ...
... To preserve the lipid fraction of the samples, the small tissue pieces were post-fixed for 1 h with osmium tetroxide (OsO 4 1%, 1.5% potassium hexacyanoferrate II in 0.1 M Sorensen phosphate buffer) under constant agitation and rinsed twice in Milli-Q water for 20 min. Using a tissue processor, the samples were then subjected to a serial dehydration in ethanol (30,70, and 100% ethanol in Milli-Q water), to facilitate a progressive Spurr resin infiltration (30,70, and 100% Spurr resin in absolute ethanol). Once infiltrated, the samples were placed into molds filled with 100% Spurr resin and cured at 60 °C for 48 h. ...
... To preserve the lipid fraction of the samples, the small tissue pieces were post-fixed for 1 h with osmium tetroxide (OsO 4 1%, 1.5% potassium hexacyanoferrate II in 0.1 M Sorensen phosphate buffer) under constant agitation and rinsed twice in Milli-Q water for 20 min. Using a tissue processor, the samples were then subjected to a serial dehydration in ethanol (30,70, and 100% ethanol in Milli-Q water), to facilitate a progressive Spurr resin infiltration (30,70, and 100% Spurr resin in absolute ethanol). Once infiltrated, the samples were placed into molds filled with 100% Spurr resin and cured at 60 °C for 48 h. ...
Background
Global warming is causing large-scale disruption of cnidarian-Symbiodiniaceae symbioses fundamental to major marine ecosystems, such as coral reefs. However, the mechanisms by which heat stress perturbs these symbiotic partnerships remain poorly understood. In this context, the upside-down jellyfish Cassiopea has emerged as a powerful experimental model system.
Results
We combined a controlled heat stress experiment with isotope labeling and correlative SEM-NanoSIMS imaging to show that host starvation is a central component in the chain of events that ultimately leads to the collapse of the Cassiopea holobiont. Heat stress caused an increase in catabolic activity and a depletion of carbon reserves in the unfed host, concurrent with a reduction in the supply of photosynthates from its algal symbionts. This state of host starvation was accompanied by pronounced in hospite degradation of algal symbionts, which may be a distinct feature of the heat stress response of Cassiopea. Interestingly, this loss of symbionts by degradation was concealed by body shrinkage of the starving animals, resulting in what could be referred to as “invisible” bleaching.
Conclusions
Overall, our study highlights the importance of the nutritional status in the heat stress response of the Cassiopea holobiont. Compared with other symbiotic cnidarians, the large mesoglea of Cassiopea, with its structural sugar and protein content, may constitute an energy reservoir capable of delaying starvation. It seems plausible that this anatomical feature at least partly contributes to the relatively high stress tolerance of these animals in rapidly warming oceans.
7jQYTVpxtJyVhU5epTFb61Video Abstract
... Transmembrane transporters involved in the distribution and assimilation of nitrogen and carbon have been identified in symbionts of the Symbiodiniaceae family (Aranda et al. 2016). Correspondingly, the animal host must be capable of internalizing photosynthates to cover its basal energetic requirements (Lampert 2016), but these are not thoroughly studied. The molecular exchange of organic compounds could be facilitated by internal membrane proteins located in the cell membranes of each symbiotic partner, and in the symbiosomal interface (Fitt and Trench 1983;Wakefield and Kempf 2001). ...
... Unlike corals, the lack of a carbonate skeleton facilitates its handling and cultivation under laboratory conditions (Ohdera et al. 2018). The adult medusa depends on the energy transferred from its symbionts to cover up to 70% of its basal needs (Lampert 2016). About 3 weeks after the symbionts are acquired by asexual polyps, depending upon symbiont species, temperature, and food intake, metamorphosis of the newly symbiotic polyp into a medusa larva occurs (Colley and Trench 1983;Fitt and Costley 1998). ...
... In the medusa Cassiopea andromeda, glucose and glycerol are the only two free carbon molecules that acquire an isotopic label in short-term studies (under 90 s), suggesting that glycerol may fuel the synthesis of lipids, being rapidly metabolized (Hofmann and Kremer 1981). Further, previous studies have shown that adult medusae lose mass (size and weight) when symbiont density declines or in the absence of light, even when food is supplemented (Lampert 2016). Apparently, when medusae shrink under low light levels, some polyunsaturated fatty acids seem to be transferred from symbiont to host (Mortillaro et al. 2009). ...
Cassiopea xamachana is a tropical medusa that lives in symbiosis with dinoflagellate algae, serving as a model organism for symbiotic studies. The symbiosis is necessary for this medusa to complete its life cycle. The symbiotic partners maintain a metabolic exchange of organic molecules that constitute an important source of energy for the animal host, with free organic molecules, like glucose and glycerol, being the primary source. This molecular exchange can be facilitated by cellular internal membrane transport proteins, such as Glucose membrane transporters (GLUTs) and Glycerol transport-like aquaglyceroporins (GLP-like), probably located at the symbiosomal interface. The present study was conducted in October 2021, evaluating the expression of transporter coding genes GLUT3, GLUT8, and GLP9 (two genes) by qPCR under conditions of symbiosis and after the loss of symbionts. Symbiotic medusae donated from Xcaret Park, Mexico (20° 34′ 24.59″ N; -87° 07′ 5.40″ W) were sampled and compared to medusae with an experimental decrease of algal symbionts. In agreement with glucose being an important mobile molecule, our results showed higher transcription levels for glucose transporters GLUT3 and GLUT8 in control compared to bleached medusae. By contrast, bleached medusae showed a higher expression of aquaglyceroporin transporters GLP9-1 and GLP9-2, probably associated with glycerol production after lipid catabolism, to compensate for lower organic carbon levels due to the loss of symbionts. Our results highlight the importance of free carbon molecules transported from symbiont to host and agree with glucose being an energy fuel for this symbiotic association.
... The results of both experiments show that the three strains belonging to clade A or B are compatible with the Cassiopea polyps, while other three strains belonging to clade C, D, or F are incompatible strains. Lampert (2016) if more than one clade was present in the water, all available clades would be found in the polyps. Our results also show that Cassiopea polyps can take up all the symbiont strains initially. ...
... So, further study is necessary to conclude whether Y106 is parasitic or not. Lampert (2016) stated that, if only one single clade of algae was present, polyps survived best with clades A or B and polyps with clade D died rather quickly. It is likely that there is difference in fitness among polyps with different strains of symbionts. ...
... The present study shows that the number of buds released from the polyps as well as the oral diameter of each polyp may be a good index to measure host fitness (Sachs and Wilcox, 2006), but that careful control of feeding regimes and light conditions as well as longer time of observation period would be necessary to study the effect of different symbiont strains on fitness of Cassiopea polyps. Cassiopea polyps would serve as a good model to investigate symbiotic relationship between cnidarian host and symbiotic algae, especially effects of different symbiont types on the fitness and stress tolerance of the holobiont (Sachs and Wilcox, 2006;Lampert, 2016;Ohdera et al., 2018). ...
The specificity of the relationship between cnidarian hosts and symbiotic dinoflagellates (zooxanthellae) differs among host species. Some cnidarian hosts can establish symbiotic relationship with various types of zooxanthellae, while others exhibit high fidelity to specific symbiont type. It is not known how compatibility or specificity of the relationship is determined. We hypothesized that some cnidarian hosts select symbiont type that leads to highest fitness when the host is flexible with symbiont type and more than one types of symbionts are available. As a first step to study this possibility, compatibility of clonal polyps of Cassiopea sp. with six strains of cultured zooxanthellae and the fitness of the host associated with different types of symbionts were studied. Polyp diameter was measured and the number of asexual buds were calculated as a measure of host fitness. The number of zooxanthellae in host and in asexual buds was also measured as a measure of symbiont fitness. Three strains KB8 (clade A), Y106 (clade A), and K100 (clade B) were compatible with the Cassiopea polyps, while other three strains, Y103 (clade C), K111 (clade D), and K102 (clade F) were incompatible. No clear difference in the fitness was found among the polyps inoculated with compatible and incompatible symbiont strains. In one experiment, a compatible strain Y106 seemed to decrease host fitness, but this should be checked by further studies. This study suggests that feeding regimes and long observation period might be important when fitness of hosts associated with different types of symbionts is investigated.
... This particular jellyfish is the only benthic semi-sessile scyphomedusa (Rhizostomeae) with a flat exumbrella that rests on the sea bottom while the subumbrella and oral arms reach into the water to obtain sufficient sunlight for algal photosymbiosis. Cassiopea hosts one or more symbiotic dinoflagellate species (Hofmann et al., 1996;Lampert, 2016) which not only provide nutrients but also act as developmental triggers (Hofmann et al., 1996;Rahat & Adar, 1980). As the only genus in the family Cassiopeidae, Cassiopea belongs to the Kolpophorae clade (Bayha et al., 2010) which exhibit a typical scyphozoan life cycle involving the following discrete stages: egg, planula, polyp, ephyra and medusa. ...
... In nature, Cassiopea species undergo obligatory symbiosis with zooxanthellae (Symbiodinaceae, dinoflagellate); this process is critical for the strobilation of polyps. Eggs and planula larvae are free of endosymbionts and polyps need to take up symbiotic algae from surrounding waters (Coffroth & Santos, 2005;Lampert, 2016). Dinoflagellates release UV-absorbing compounds that protect the host from harmful solar UV radiation (Banaszak & Trench, 1995) and also help the host to adapt to changes in temperature, salinity and light (Mellas et al., 2014). ...
... Dinoflagellates release UV-absorbing compounds that protect the host from harmful solar UV radiation (Banaszak & Trench, 1995) and also help the host to adapt to changes in temperature, salinity and light (Mellas et al., 2014). Symbiotic zooxanthellae can also provide nutrients (sugar, fatty acids) to their host (Lampert, 2016). This may explain why our algal-free polyps were smaller than the normal symbiotic polyps under the same feeding regime. ...
The upside-down jellyfish Cassiopea has become a model organism for the study of symbiosis between dinoflagellates and cnidarian hosts. Most previous studies have indicated that the presence of symbiotic zooxanthellae is a key requirement for strobilation in Cassiopea. Indole compounds have been shown to induce strobilation in many scyphozoans, including symbiotic Cassiopea xamachana. To determine if indoles could induce aposymbiotic Cassiopea polyp strobilation, we acquired algal-free Cassiopea andromeda polyps and used three indoles (indomethacin, 2-methyl indole, and 5-methoxy-2-methyl indole) to induce metamorphosis by applying single doses within a range of 0.005–100 μM. Analysis showed that indoles successfully induced aposymbiotic polyp strobilation and that the induction effects were compound- and dose-dependent. 5-Methoxy-2-methyl indole and 2-methyl indole were significantly more effective than indomethacin (P < 0.001). Data showed that it took 3 to 9 days for 5-methoxy-2-methyl indole or 2-methyl indole to induce strobilation and that 25 μM of 2-methyl indole was the most effective inducer of strobilation in algae-free C. andromeda polyps. Indole-induced strobilation was associated with several developmental abnormalities, including failed or retarded regeneration of residual polyps after strobilation, a reduction in the size of ephyrae, and abnormal morphology of the ephyrae.
... The mutualistic endosymbiosis between marine invertebrates and photosynthetic dinoflagellates represents one of the most important associations in tropical marine environments, allowing the growth of diverse, healthy and productive marine ecosystems, including coral reefs (Done et al., 1996;Knowlton et al., 2010;Davy et al., 2012;de Groot et al., 2012;Fransolet et al., 2012;Kennedy et al., 2013). Dinoflagellates of the family Symbiodinaceae [formerly Symbiodinium; see the recent revision by LaJeunesse et al. (2018) are the most common group of symbionts found in tropical symbiotic invertebrates (LaJeunesse, 2001), such as corals, sea anemones, jellyfish, and clams (Lampert, 2016)]. Endosymbiotic relationships involving symbiotic dinoflagellates first evolved in the Triassic period (Muscatine et al., 2005) and are essential contributors to global primary production, accounting for 1-10% of the total benthic production (Muscatine, 1990). ...
... Cassiopea sp. was chosen as a model symbiotic cnidarian species for our study as it is a benthic scyphozoan (Rhizostomae) inhabiting subtropical and tropical coastal shallow waters, especially mangroves and seagrass meadows (Lampert, 2016;Klein et al., 2017;Ohdera et al., 2018). In these environments they are exposed to extreme conditions, including fluctuations of O 2 and pH in the environment (Gray et al., 2012). ...
... Additionally, Cassiopea sp. harbors populations of Symbiodiniaceae, which are mostly concentrated in its oral arms (Hofmann et al., 1996;Lampert, 2016). The Cassiopea-Symbiodiniacea association is thus an example of successful cooperation under potentially stressful conditions, that is becoming increasingly popular as a model species. ...
The characterization of the internal microenvironment of symbiotic marine invertebrates is essential for a better understanding of the symbiosis dynamics. Microalgal symbionts (of the family: Symbiodiniaceae) influence diel fluctuations of in host O2 and pH conditions through their metabolic activities (i.e., photosynthesis and respiration). These variations may play an important role in driving oxygen budgets and energy demands of the holobiont and its responses to climate change. In situ measurements using microsensors were used to resolve the O2 and pH diel fluctuations in the oral arms of non-calcifying cnidarian model species Cassiopea sp. (the “upside-down jellyfish”), which has an obligatory association with Symbiodiniaceae. Before sunrise, the internal O2 and pH levels were substantially lower than those in ambient seawater conditions (minimum average levels: 61.92 ± 5.06 1SE μmol O2 L–1 and 7.93 ± 0.02 1SE pH units, respectively), indicating that conditions within Cassiopea’s oral arms were acidified and hypoxic relative to the surrounding seawater. Measurements performed during the afternoon revealed hyperoxia (maximum average levels: 546.22 ± 16.45 1SE μmol O2 L–1) and internal pH similar to ambient levels (8.61 ± 0.02 1SE pH units). The calculated gross photosynthetic rates of Cassiopea sp. were 0.04 ± 0.013 1SE nmol cm–2 s–1 in individuals collected at night and 0.08 ± 0.02 1SE nmol cm–2 s–1 in individuals collected during the afternoon.
... Other symbiont-bearing cnidarians are available (e.g., zoanthids, anemones, and soft corals-see Stat et al. 2006) and among them is the benthic jellyfish Cassiopea andromeda, an invasive species that is easily maintained and bred in laboratory conditions (Hofmann et al. 1996;Holland et al. 2004;Pierce 2005). This species also associates with Symbiodiniaceae in a similar fashion to corals and is used as a model organism for experimental ecology (Lampert 2016;Ohdera et al. 2018;Newkirk et al. 2020). ...
... After strobilation, the newly released ephyrae were divided into two groups. The first group was kept for approximately 8 weeks with adult jellyfish to stimulate the horizontal acquisition of symbionts (see Sachs and Wilcox 2006;Mellas et al. 2014;Lampert 2016). The other group was kept in artificial seawater in the same conditions as previously mentioned and harbored only vertically transmitted symbionts. ...
... seems more tolerant to heat than to cold stress (Aljbour et al. 2019). Therefore, Cassiopea may be an excellent model for investigations on the evolution of cnidarian-algal symbioses (Lampert 2016;Ohdera et al. 2018) and also for physiological tolerance to heat. However, it may not be a good model for climate change investigations considering the IPCC scenarios, because it is not sensitive enough. ...
Oceans are undergoing successive heatwaves. Several invertebrate taxa associate with dinoflagellates and are susceptible to bleaching caused by heat stress. Although the impacts of a single bleaching event have been well documented, the consequences of successive events are less understood. We investigated the effects of multiple thermal stress events on juvenile Cassiopea andromeda, while also addressing the roles of symbiont concentration and heterotrophic diet regimen. We exposed medusae with two distinct symbiont concentrations (high and low) and under two feeding frequencies (Artemia offered daily and every 3 days) to three thermal stress events and at three temperatures (control of 27 °C, and treatments of 30 and 33 °C) while recording proportional changes in chlorophyll-a and jellyfish growth. Results show that 30 and 33 °C were not enough to trigger bleaching and did not affect growth. Symbiont concentration also did not affect growth, but medusae with higher symbiont concentration displayed higher chlorophyll-a loss. Diet regimen had little impact on chlorophyll-a variation, but had a dramatic effect on growth, as medusae fed daily grew, while those fed every 3 days shrank. These findings show that it is not possible to evaluate if C. andromeda becomes more resilient after successive thermal stress episodes, because even 33 °C did not generate enough stress. Therefore, C. andromeda juveniles are thermotolerant and may not serve as a good model for investigations on the resilience of coral reef zooxanthellate fauna to the current climate change predictions. Finally, at this life stage, the symbiotic relationship seems less important for growth than heterotrophy.
... harbor dense intracellular populations of Symbiodiniaceae spp. and inhabit shallow tropical and sub-tropical waters (Lampert, 2016). Cassiopea spp. ...
... Cassiopea spp. are considered robust cnidarians because they can persist under a broad range of temperature and salinity conditions (Klein et al., 2016a;Morandini et al., 2017) and are prevalent in shallow lagoon systems (Lampert, 2016). These habitats are often characterized by intense light and variable yet elevated temperatures in summer relative to other well-flushed coastal waters. ...
... For example, on small spatial scales, corals that live in more variable temperature environments are more tolerant to thermal extremes than conspecifics that inhabit less thermally variable sites (Thompson and Van Woesik, 2009;Barshis et al., 2013;Schoepf et al., 2015). Cassiopea spp., including those studied here from the central Red Sea, often inhabit shallow waters, characterized by high levels of UV radiation and temperature variability (McGill and Pomory, 2008;Lampert, 2016). Thus, it is reasonable to hypothesize that extreme and variable thermal conditions within such habitats contribute to the acquired thermal resilience of Cassiopea-Symbiodiniaceae associations (Ohdera et al., 2018). ...
Responses of cnidarian-Symbiodiniaceae associations to warming are determined, in part, by high-frequency temperature variability. Yet, the role of such variability in determining specific maximum temperature thresholds of cnidarian holobionts (the ecological units comprised of cnidarian hosts and associated microorganisms, including Symbiodiniaceae) remains untested. Here we contrasted the thermal resilience (that is the ability to resist stress) of a model symbiotic cnidarian from the Red Sea (jellyfish of the genus Cassiopea) under stable and diel oscillating temperature conditions that provide night-time reprieves from daily maximum temperatures. Holobionts were subjected to two thermal trajectories; one that increased but plateaued at 2°C below identified bleaching thresholds and another that increased incrementally until holobionts bleached. We used behavior, growth, photochemical efficiency, Symbiodiniaceae (symbiont) cell density, and total chlorophyll cell content to characterize thermal resilience and examined Symbiodiniaceae community composition responses at 1 and 13 days of exposure, and post-bleaching. Lower night-time temperatures, resulting in lower daily mean temperatures, allowed holobionts to withstand daily maximum temperatures close to their bleaching thresholds for two extra days than those under stable maximum temperature conditions. Lower night-time temperatures increased the bleaching threshold of the holobionts, whereby holobionts exposed to night-time thermal reprieves tolerated a more extreme daily mean temperature of 40.6°C and reached a daily thermal maxima 4°C higher than those under stable temperature conditions. However, post-bleaching observations indicate that night-time temperature reprieves did not prevent symbiont cell or pigment loss. Symbiodiniaceae communities were unaffected by lower night-time temperatures and no directional changes indicative of symbiont shuffling/selection of thermally tolerant lineages were observed. We show that stable experimental treatments may fail to accurately identify maximum thermal thresholds of non-calcifying cnidarians and limit their relevance to in situ environments that are often characterized by high levels of temperature fluctuations.
... are unique among scyphomedusae in that their characteristic flat exumbrella rests on the sea bottom, while their convex subumbrella and oral arms face upwards. High light penetrance is important for species within this genus, as the jellyfish hosts one or more photosynthetic dinoflagellate species of the genus Symbiodinium Lampert, 2016). Similar to their coral relatives, nutrient exchange is a key component supporting this cnidarian-dinoflagellate mutualism (Hofmann and Kremer, 1981;Welsh et al., 2009;Freeman et al., 2016). ...
... rely on the symbionts as a developmental trigger (Hofmann et al., 1978;Colley and Trench, 1985). A fascination with these requisite traits of the upsidedown jellyfish has fueled studies on the Cassiopea-Symbiodinium interaction since the 1980s (see recent review by Lampert, 2016). While its efficacy as a system for symbiosis research is well known in the literature, Cassiopea is gaining momentum as a model species in other areas. ...
... While aposymbiotic polyps can be propagated as described above, symbiotic polyps can be generated by providing the polyps with Symbiodinium spp. Cassiopea polyps are capable of forming associations with virtually all symbiotic Symbiodinium cultures Lampert, 2016), making this an ideal system for comparative studies. The colonization characteristics of Cassiopea provide two tractable phenotypes to visually confirm variation in the symbiotic association. ...
The upside-down jellyfish Cassiopea xamachana (Scyphozoa: Rhizostomeae) has been predominantly studied to understand its interaction with the endosymbiotic dinoflagellate algae Symbiodinium. As an easily culturable and tractable cnidarian model, it is an attractive alternative to stony corals to understanding the mechanisms driving establishment and maintenance of symbiosis. Cassiopea is also unique in requiring the symbiont in order to complete its transition to the adult stage, thereby providing an excellent model to understand symbiosis-driven development and evolution. Recently, the Cassiopea research system has gained interest beyond symbiosis in fields related to embryology, climate ecology, behavior, and more. With these developments, resources including genomes, transcriptomes, and laboratory protocols are steadily increasing. This review provides an overview of the broad range of interdisciplinary research that has utilized the Cassiopea model and highlights the advantages of using the model for future research.
... Symbiont-bearing jellyfish in the genus Cassiopea exhibit a conspicuous lifestyle by settling upside-down on sediment, exposing the subumbrella and oral arms to light. The oral side (i.e., the subumbrella side) of the medusa is particularly dense in intracellular microalgal symbionts, which are dinoflagellates of the family Symbiodiniaceae (Lampert, 2016). In contrast to corals where symbionts are found in endoderm cells, symbiont algae in Cassiopea are kept in clusters in host-specialized amoebocyte cells, directly below the epidermis in the mesoglea of the bell and oral arms (Colley and Trench, 1985;Estes et al., 2003). ...
... A more pronounced depletion of O 2 was observed in the top 1 mm of the bell after 50 min darkness. The higher O 2 consumption near the subumbrella epidermis probably reflects the presence of abundant musculature required for bell pulsation and motility of jellyfish (Blanquet and Riordan, 1981;Thuesen et al., 2005;Aljbour et al., 2017), as well as the presence of a dense population of endosymbionts (Estes et al., 2003;Lampert, 2016). Both have previously been ascribed to heavy diel fluctuations of O 2 measured in Cassiopea oral arms (Arossa et al., 2021). ...
Introduction
The jellyfish Cassiopea has a conspicuous lifestyle, positioning itself upside-down on sediments in shallow waters thereby exposing its photosynthetic endosymbionts (Symbiodiniaceae) to light. Several studies have shown how the photosymbionts benefit the jellyfish host in terms of nutrition and O2 availability, but little is known about the internal physico-chemical microenvironment of Cassiopea during light–dark periods.
Methods
Here, we used fiber-optic sensors to investigate how light is modulated at the water-tissue interface of Cassiopea sp. and how light is scattered inside host tissue. We additionally used electrochemical and fiber-optic microsensors to investigate the dynamics of O2 and pH in response to changes in the light availability in intact living specimens of Cassiopea sp.
Results and discussion
Mapping of photon scalar irradiance revealed a distinct spatial heterogeneity over different anatomical structures of the host, where oral arms and the manubrium had overall higher light availability, while shaded parts underneath the oral arms and the bell had less light available. White host pigmentation, especially in the bell tissue, showed higher light availability relative to similar bell tissue without white pigmentation. Microprofiles of scalar irradiance into white pigmented bell tissue showed intense light scattering and enhanced light penetration, while light was rapidly attenuated over the upper 0.5 mm in tissue with symbionts only. Depth profiles of O2 concentration into bell tissue of live jellyfish showed increasing concentration with depth into the mesoglea, with no apparent saturation point during light periods. O2 was slowly depleted in the mesoglea in darkness, and O2 concentration remained higher than ambient water in large (> 6 cm diameter) individuals, even after 50 min in darkness. Light–dark shifts in large medusae showed that the mesoglea slowly turns from a net sink during photoperiods into a net source of O2 during darkness. In contrast, small medusae showed a more dramatic change in O2 concentration, with rapid O2 buildup/consumption in response to light–dark shifts; in a manner similar to corals. These effects on O2 production/consumption were also reflected in moderate pH fluctuations within the mesoglea. The mesoglea thus buffers O2 and pH dynamics during dark-periods.
... The genus Cassiopea Peron and Lesueur 1810 consists of twelve species, known as the upside-down jellyfish, a benthic scyphozoan (Rhizostomeae), which is found in symbiosis with dinoflagellates of the genus Symbiodinium (Lampert, 2016). Unlike other jellyfish, these coelenterates exhibit an epibenthic lifestyle with their inverted bell on the substrate and upward-facing oral arms, which is an adaptation to symbiosis with dinoflagellates (Lampert, 2016). ...
... The genus Cassiopea Peron and Lesueur 1810 consists of twelve species, known as the upside-down jellyfish, a benthic scyphozoan (Rhizostomeae), which is found in symbiosis with dinoflagellates of the genus Symbiodinium (Lampert, 2016). Unlike other jellyfish, these coelenterates exhibit an epibenthic lifestyle with their inverted bell on the substrate and upward-facing oral arms, which is an adaptation to symbiosis with dinoflagellates (Lampert, 2016). These jellyfish harbor an abundant community of symbionts, which together with their lifestyle favour light uptake by symbionts (Verde & McCloskey, 1998). ...
Upside-down jellyfish are a group of benthic scyphozoans belonging to the genus Cassiopea, whose members are in symbiosis with dinoflagellates and inhabit tropical and subtropical waters. Although there are some studies of the genus in the Caribbean, these are limited. In Cuba, the group's studies are restricted to reports on taxonomic lists and, as far as we know, no one has performed any analyzes of the densities of these jellyfish in seagrass or mangrove ecosystems in Cuba. In this work, the populations of Cassiopea spp. in Jardines de la Reina National Park (JRNP) were characterized, for the first time for this Marine Protected Area and Cuba. One hundred 1m2 square frames were placed at 14 JRNP sites. For each site, the species, density, size of the individuals, and abiotic factors were determined. Density and diameter comparisons were made between sites, zones, and regions within the JRNP. The percentage of the benthic cover was determined and a correlation was made between density and diameter. A total of 10,803 individuals were recorded, of which 7,618 belong to Cassiopea xamachana and 3,185 belong to Cassiopea frondosa. Both species share a niche and no evident segregation was detected according to abiotic variables. Significant differences were detected in comparisons of density and size across sites and zones. Density and size in the JRNP were negatively correlated, and higher aggregations of the species were observed at lower sizes. Density mean values ranged from 2.18 to 14.52 ind. /m 2 with maximum values of 79 ind. /m 2. Cayo Alcatraz was the site found to have the highest density while Cachiboca was the site with the lowest density. The average bell diameter size of the individuals ranged from 9.34 to 15.31 cm for the sampled sites, with minimum and maximum values of 2.5 cm and 32.6 cm. The smallest size was recorded at Cayo Alcatraz while the largest size was reported for Boca de las Anclitas. The environmental factors evaluated showed no significant relationship with the density or diameter of Cassiopea, while the Thalassia testudinum cover was negatively correlated with Cassiopea density at all fourteen sites in the JRNP. The percentage of Cassiopea coverage was higher than those reported in the literature, with four sites exceeding 20% coverage. In general, the populations of Cassiopea spp. in the JRNP did not differ greatly, although a higher density was observed towards the eastern region of the park. It was shown for the first time for the species that density and size have a negative correlation. Future studies are required to quantify the impact of Cassiopea on coastal marine ecosystem processes and to further determine how anthropogenic changes may be altering the function of these tropical ecosystems.
... Cassiopea xamachana is a benthic jellyfish that lives in ecologically obligate symbiosis with the photosynthetic dinoflagellate Symbiodinium microadriaticum (Colley and Trench, 1983;Lampert, 2016). The adult medusa rests on the sea bottom, their convex umbrella and oral arms facing upwards to allow the capture of light by their symbionts (Lampert, 2016;Ohdera et al., 2018). ...
... Cassiopea xamachana is a benthic jellyfish that lives in ecologically obligate symbiosis with the photosynthetic dinoflagellate Symbiodinium microadriaticum (Colley and Trench, 1983;Lampert, 2016). The adult medusa rests on the sea bottom, their convex umbrella and oral arms facing upwards to allow the capture of light by their symbionts (Lampert, 2016;Ohdera et al., 2018). The colonization by algal symbionts supports the transition from polyp to adult medusa (Hofmann et al., 1996;Newkirk et al., 2018). ...
Cassiopea xamachana is a model system for studies in animal symbiosis with algal symbionts. This medusa is also associated with a microbial community that can impact its health, but this community has not been thoroughly studied. Shifts in the bacterial community following the loss of symbionts involving stress, environmental changes, or seasonal fluctuations can be complex, as the role of symbionts in structuring this community is not well established. To understand the interplay among microbial associates with this host, we explored the experimental diminishing of algal symbionts, and the influence of seasonal fluctuations over the structure of the bacterial community, through 16S rRNA gene high-throughput sequencing. Results showed that Gammaproteobacteria, Bacteroidia, and Alphaproteobacteria were dominant in all the mucus samples at the beginning of the experiments. However, after 28 days, bleached medusas showed a marked increase in Gammaproteobacteria, specifically in the genus Vibrio, as evidenced by Linear Discriminant Analysis of Effect Size (LEfSe). Seasons also resulted in shifts of the bacterial community, although bacterial genera were distinct from those found in bleached medusas, suggesting temporal associations with the host. According to PERMANOVA analysis, seasonal fluctuations affected the dominant bacterial members (p = 0.07), but symbiont presence was a more significant driver (p=0.001). We found the bacterial community of C. xamachana is like that of other jellyfish and corals, which furthers the interest in this animal as a study model. Defining relevant bacterial genera can help us understand the functional role of the holobiont members that assemble and maintain a healthy microbial community. Also, studies in other regions where C. xamachana distributes can help us define a core bacterial community for this medusa.
... Of the 79 valid genera in Scyphozoa, only 11 harbour symbionts: Linuche, Nausithoe (Coronamedusae), Bazinga, Cephea, Cassiopea, Cotylorhiza, Netrostoma, Mastigias, Phyllorhiza, Thysanostoma, and Versugia, most belonging to the suborder Kolpophorae and all of which with a metagenic life cycle (Djeghri et al., 2019). The best-studied genus among the zooxanthellate Scyphozoa is Cassiopea, with its symbionts serving as a holobiont model to reveal various aspects of their mutualism (Lampert, 2016;Ohdera et al., 2018). The symbionts of the species Cotylorhiza tuberculata (Macri, 1779) and Phyllorhiza punctata (von Lendenfeld, 1884) have not yet been described in detail (LaJeunesse et al., 2021). ...
... All of the species investigated in the present study have a metagenic life that includes a scyphistoma, strobilation reproduction, and adult medusae, which reproduce sexually and produce planulae that develop into polyps. According to experimental models, Cassiopea polyps show extreme flexibility in the types of symbionts they acquire from free-living species in their external environment (Mellas et al., 2014;Lampert, 2016;Newkirk et al., 2018). Free-living species of Symbiodiniaceae provide the largest reservoir of symbiotic cells (Coffroth et al., 2006;Pochon & Gates, 2010;Newkirk et al., 2018). ...
Symbiotic scyphozoan jellyfish are poorly understood in terms of their symbionts and traits, as well as the ecological significance of this association. Dinoflagellate symbionts of the medusae Cotylorhiza tuberculata, Phyllorhiza punctata, and Cassiopea xamachana collected in the Mediterranean Sea and Cabo Frio (Rio de Janeiro, Brazil) were phylogenetically identified based on 28S rDNA and ITS2 haplotypes. The studied medusae harbour only one phylotype of symbionts in a time, but scyphozoan jellyfishes can associate with several types of symbionts. This study confirmed that the main symbionts of investigated scyphozoans belong to the genera Symbiodinium, Philozoon, and Breviolum. The associations between dinoflagellate symbionts and Cotylorhiza tuberculata changed from year to year, hosting Philozoon one year and Breviolum another. Invasive species in the Mediterranean Sea Phyllorhiza punctata harboured dinoflagellate symbionts of genus Symbiodinium as in the native areal. Pigment analysis of two shallow-water symbiont species Breviolum sp. and Philozoon medusarum revealed characteristic profiles for each genus.
... life cycle and invasion success because it modulates several stages of development for both asexual and sexual reproduction, including strobilation, larval settlement and metamorphosis (Fitt and Costley, 1998;Hofmann et al., 1996;Newkirk et al., 2018). In addition, temperature affects symbiont concentration in the jellyfish tissue because warmer conditions may induce bleaching (McGill and Pomory, 2008;Lampert, 2016;Newkirk et al., 2018;Klein et al., 2019). Salinity is also an important modulator of Cassiopea spp. ...
... Besides temperature and salinity, variations in other environmental parameters may also play a relevant role in the physiology and ecology of Cassiopea jellyfish. For instance, increase in nutrients, chlorophyll-a (chl-a), and organic matter often enhance both heterotrophic feeding and the photoautotrophy performed by their endosymbionts (Welsh et al., 2009;Stoner et al., 2011Stoner et al., , 2016Lampert, 2016;Freeman et al., 2017;Ohdera et al., 2018;Djeghri et al., 2020). Therefore, fluctuations in all of these parameters due to natural conditions and/or human activities may stimulate either an increase or decrease in Cassiopea spp. ...
Cassiopea jellyfish have successfully invaded several marine ecosystems worldwide. We investigated if Cassiopea andromeda grows larger (umbrella size) and if their populations are more stable in shrimp farms than in mangroves in the Brazilian coast. Our results show that jellyfish abundance is higher in the shrimp farm during the rainy season and in the mangrove during dry season. The population is stable during both seasons in the shrimp farm, but unstable in the mangroves, as jellyfish are absent during rainy season. Shrimp farm-associated jellyfish are three times larger than those in the mangroves, regardless of season. We recorded the largest (49.2 cm of umbrella diameter) ever C. andromeda individual in the shrimp farm. Unlike the mangroves, the shrimp farm provides environmental intra-annual stability that promotes jellyfish growth and population persistence. Therefore, C. andromeda populations can be seasonally dynamic and artificial environments such as aquaculture facilities may facilitate the invasion process.
... Indeed, Cassiopea spp. polyps have been successfully infected with a variety of isolated and mixed Symbiodiniaceae genera including Symbiodinium, Cladocopium, Breviolum (previously Symbiodinium clade B) and Durusdinium (previously Symbiodinium clade D) Mellas et al. 2014;Lampert 2016). However, adult medusae tend to harbour only one phylotype of symbiont suggesting that a mechanism such as competitive exclusion occurs within the host . ...
... Moreover, the zooxanthellae Durusdinium (previously Symbiodinium clade D) can increase the mortality of Cassiopea sp. polyps (Lampert 2016). All these suggest that, at the polyp stage, symbionts and autotrophy are of little direct importance for most zooxanthellate jellyfishes. ...
Many marine organisms form photosymbioses with zooxanthellae, but some, such as the medusozoans, are less well known. Here, we summarize the current knowledge on the diversity of zooxanthellate jellyfishes, to identify key traits of the holobionts, and to examine the impact of these traits on their ecology. Photosymbiosis with zooxanthellae originated at least seven times independently in Medusozoa; of these, five involve taxa with medusae. While most zooxanthellate jellyfishes are found in clades containing mainly non-zooxanthellate members, the sub-order Kolpophorae (Scyphozoa: Rhizostomeae) is comprised—bar a few intriguing exceptions—of only zooxanthellate jellyfishes. We estimate that 20–25% of Scyphozoa species are zooxanthellate (facultative symbiotic species included). Zooxanthellae play a key role in scyphozoan life-cycle and nutrition although substantial variation is observed during ontogeny, or at the intra- and inter-specific levels. Nonetheless, three key traits of zooxanthellate jellyfishes can be identified: (1) zooxanthellate medusae, as holobionts, are generally mixotrophic, deriving their nutrition both from predation and photosynthesis; (2) zooxanthellate polyps, although capable of hosting zooxanthellae rarely depend on them; and (3) zooxanthellae play a key role in the life-cycle of the jellyfish by allowing or facilitating strobilation. We discuss how these traits might help to explain some aspects of the ecology of zooxanthellate jellyfishes—notably their generally low ability to outbreak, and their reaction to temperature stress or to eutrophication—and how they could in turn impact marine ecosystem functioning.
... Also, the polyps grown in the aquarium hosted S. necroappetens (clade A13), suggesting the presence of this zooxanthellae species in the seawater used in aquarium management. Actually, polyps acquire the clade available in the water, and they have a higher chance of survival and of having strobilation if they acquire clade A or B than other clades [65]. ...
The zooxanthellate jellyfish Cassiopea andromeda (Forsskål, 1775), a Lessepsian species increasingly common in the western and central Mediterranean Sea, was investigated here to assess its potential as a source of bioactive compounds from medusa specimens both collected in the wild (the harbor of Palermo, NW Sicily) and reared under laboratory-controlled conditions. A standardized extraction protocol was used to analyze the biochemical composition of the two sampled populations in terms of protein, lipid, and pigment contents, as well as for their relative concentrations of dinoflagellate symbionts. The total extracts and their fractions were also biochemically characterized and analyzed for their in vitro antioxidant activity to quantify differences in functional compounds between wild and reared jellyfish. The two populations were similar in terms of extract yield, but with substantial differences in biomass, the number of zooxanthellae, protein and lipid contents, and fatty acid composition. The hydroalcoholic extracts obtained from jellyfish grown under controlled conditions showed greater antioxidant activity due to the presence of a higher content of bioactive compounds compared to wild jellyfish. This study could be the basis for considering the sustainable breeding of this holobiont or other similar organisms as a source of valuable compounds that can be used in the food, nutraceutical, or pharmaceutical sectors.
... While laboratory-based research has laid the foundation for detailed understanding of the life history of Cassiopea, field research is essential to understanding ecological dynamics on a broader scale. For example, the scyphistomae acquire symbionts through uptake during filter feeding (referred to as horizontal transfer; Fitt et al. 1987, Fitt and Costley 1998, Lampert 2016. The intricate nature of the Cassiopea-Symbiodiniaceae relationship, its significance in the overall life cycle, and the specific mechanisms of symbiont acquisition underscore the necessity for ongoing field research. ...
Research on upside-down jellies has largely focused on their life history and symbiotic relationship with members of the Symbiodiniaceae, with most studies carried out in laboratory settings. Members of the genus Cassiopea have been studied widely for their semi-sessile benthic behavior and for hosting algal symbionts analogous to their anthozoan counterparts, stony coral, making them excellent laboratory models to study host-symbiont relationships. Much less information is available on their field ecology, though high population densities of upside-down jellies have been linked with human activity in nearshore environments. In this review, we searched readily available literature on Cassiopea with the goal to identify major gaps in understanding their field ecology. Internet-based searches using the Web of Science Core Collection through October 2023 yielded 195 documents on Cassiopea research, with 72% of the published studies laboratory-based and the remainder including field studies and reviews. While historical papers date back to 1774, there are generally fewer than 10 per decade, until 1990, with a subsequent exponential increase in publications. Publications based on field studies became more frequent beginning in the early 2000s. This literature review provides a baseline for understanding the existing realm of Cassiopea research and indicates that field-based studies could enhance understanding of their responses in anthropogenically-impacted environments. Why Scientometrics?-Scientometrics involve the study of quantitative aspects of the process of science as a communication system, concerned with the analysis of citations in the academic literature (Bornmann and Leydesdorff 2014, Mingers and Leydesdorff 2015). This approach serves to evaluate and identify gaps in the literature of an area of study, while supporting the in-depth review of existing literature (Ouyang et al. 2018, Ren et al. 2021). The evaluation of articles utilizing this methodology has yielded creative perspectives by employing quantitative analysis to examine the dynamics and advancements in scientific endeavors, including input, output,
... The resultant strongly interdependent organism-unit is referred to as a 'holobiont'. As the C. andromeda holobiont is specialized to provide optimal growing conditions and protection for the dinoflagellates, these microalgae can readily proliferate in this host habitat (Lampert, 2016;Djeghri et al., 2019). ...
Introduction
The up-side down jellyfish Cassiopea andromeda represents a yet untapped marine species that could be targeted as a new source for functional ingredients, such as natural pigments and antioxidants. Since C. andromeda hosts endosymbiotic dinoflagellates, this jellyfish contains peridinin pigments, which are linked with high antioxidant capacities and many other health-promoting properties. This study investigates the potential to specifically increase the content of peridinin and overall antioxidant activity in C. andromeda, through the targeted application of different photosynthetic active radiation (PAR) intensities and ultraviolet radiation, cultured in fully controlled indoor aquaculture systems.
Materials and Methods
Indoor bred C. andromeda specimens were exposed to five different PAR intensities (50, 100, 200, 400 and 800 µmol photons m⁻² s⁻¹) and a combined treatment of narrow-band UVB (λ = 285 ± 10 nm) radiation and intermediate (200 µmol photons m⁻² s⁻¹) PAR intensity over a period of four weeks. Before the treatment and after two- and four-week treatment intervals, pigment concentrations and antioxidant activity levels were measured using high-performance liquid chromatography (HPLC) and the Trolox Equivalent AntioxidantCapacity (TEAC) assay, respectively. In addition, relative growth rate, umbrella pulsation and photosynthetic efficiency (measured by pulse amplitude modulated fluorometry) of C. andromeda individuals were also monitored throughout the experiment.
Results
Chlorophyll a (Chl a) and peridinin (Per) dominated overall pigment content in C. andromeda endosymbionts, chlorophyll c2 and diadinoxanthin were detected in minor amounts. Over the treatment time, Chl a and Per concentrations, measured as µg g⁻¹ jellyfish dry weight and pg microalgae-cell⁻¹, decreased sharply at higher PAR intensities (200 – 800 µmol photons m⁻² s⁻¹) compared to the control treatment (100 µmol photons m⁻² s⁻¹). After four weeks Chl a and Per concentrations were lowest at the highest PAR intensity (800 µmol photons m⁻² s⁻¹) and highest at the lowest PAR intensity (50 µmol photons m⁻² s⁻¹). Moreover, the ratio of Chl a and Per showed a relative decrease of Per with increasing PAR intensity. The combined treatment of narrow-band UVB (λ = 285 ± 10 nm) radiation and intermediate (200 µmol photons m⁻² s⁻¹) PAR intensity led to significantly elevated Chl a and Per concentrations compared to the 200 µmol photons m⁻² s⁻¹ PAR treatment without UVB. Significantly elevated antioxidant activity levels, measured as Trolox Equivalents mmol g⁻¹ jellyfish dry weight, were only detected in UVB exposed C. andromeda, indicating that Chl a and Per did not determine overall antioxidant capacity. The photosynthetic efficiency of C. andromeda endosymbionts was not affected by elevated antioxidant activity. Opposing that, the jellyfish hosts that were exposed to the UVB treatment shrunk drastically, indicating a strong stress response.
Discussion
With this study, we demonstrate for the first time the application potential of PAR intensity manipulations and UVB irradiation, to increase the content of valuable pigments and antioxidants in C. andromeda jellyfish and their endosymbiotic dinoflagellates that live in hospite within the host tissue. Based on these findings, we propose the culture of C. andromeda under fully controlled and light-optimized conditions as new pathway to harness bioproducts and functional ingredients.
... An exceptionally high regenerative capacity was observed for the jellyfish Cassiopea (Zeleny, 1907;Stockard, 1910;Cary, 1916;Gamero-Mora et al., 2019). These jellyfish exhibit a unique benthic lifestyle (Bigelow, 1900), which gave them their colloquial name the "upside-down jellyfish", and live in a close symbiotic relationship with photosynthetic dinoflagellates from the family Symbiodiniaceae (Thornhill et al., 2006;Lampert, 2016;LaJeunesse et al., 2018). They occur cosmopolitan in both tropical and subtropical coastal ecosystems (Morandini et al., 2017;Ohdera et al., 2018). ...
The upside-down jellyfish Cassiopea increasingly occurs in many (sub-) tropical coastal habitats such as mangrove forests, seagrass meadows, and coral reefs. Its mixotrophic lifestyle and ecophysiological plasticity as well as a high regenerative capacity may be reasons for its success. While the regeneration of umbrella tissue and body structures (i.e. rhopalia and oral arms) was already demonstrated, it remains unclear whether a fully functioning medusa can regenerate from only umbrella tissue. In this study, we thus investigated the regeneration of umbrella fragments over time. We conducted a laboratory experiment for which we used 18 Cassiopea medusae of three different size classes that were cut into two pieces each, one fragment with oral arms and one without. Over a total observation period of 5 weeks, we regularly monitored survival, pulsation behavior, growth and the regeneration pattern of fragments. Findings revealed that 100% of the fragments with oral arms and 88% of the fragments without oral arms survived. Pulsation behavior occurred in all fragments and lasted until the end of the experiment in 94% of all fragments. The umbrella area of fragments without oral arms showed a significantly higher decrease in the first two weeks compared to fragments with oral arms. A complete regeneration of umbrella tissue was observed in all fragments, with and without oral arms alike, and 50% of all fragments even regenerated rhopalia or oral arms as body structures after 33 days. These results suggest an outstanding regenerative capacity of Cassiopea jellyfish after fragmentation. This may contribute to (i) explain the currently observed success of upside-down jellyfish and (ii) extend our knowledge about its regeneration process, which might even act as an asexual reproduction mode in Cassiopea.
... In the presence of Symbiodinium, sea jelly tentacles exhibit various color morphs and in their polyp stages, Sea jelly is capable to directly uptake the Symbiodinium from the water column. Thereby the sea jelly of the Red sea exclusively harbored Symbiodinium clade A1 (Lampert 2016). ...
The endosymbionts of Symbiodiniaceae members establish an obligate relationship with most of the reef-building corals. Photosynthates of Symbiodiniaceae symbionts provide the maximum energy requirements of the host coral. Apart from the coral growth benefits, the mutual relationship extends to respond the environmental stress as well. Coral-endosymbiont mutualism is affected by various stress factors such as light, salinity, temperature, and eutrophication. However, the coral-algal symbionts adaptation to these rapid environmental changes is not much studied. Algal endosymbionts are classified into nine clades by genus level (major scleractinian corals – Clade A-D). These clades are named A to I with many subclades being presented in each clade that was identified based on the genetic marker ITS sequences, from which few are found tolerant to adverse conditions. This suggested that coral susceptibility or resistance to stress depends on the type of clade they harbor. Also, the prolonged environmental conditions may bring evolutionarily diverse clade lineages enabling corals to attain stress tolerance to temperature, UV, and high salinity. Thus, the present study may aid in understanding the coral-algal mutualistic adaptations under various stress conditions.
... The exception amongst pulsating jellyfish may be the results in Cassiopea sp., which presented ratios R: of approximately 0.17 ± 0.02 (Aljbour et al., 2017). These upside-down jellyfish have a more benthic lifestyle with a strong reliance for food on its symbiotic dinoflagellate (Lampert, 2016). Hence, their pulsation is less locomotive and the presence of these autotrophs may increase the ETS activity measured, leading to a higher (Bondyale-Juez et al., 2017). ...
Physalia physalis and Velella velella, are among the few marine organisms that harness the wind for their locomotion, whereas other cnidarian jellyfish make use of their pulsating bell-shaped bodies to propel themselves through the seas. We investigate their composition and metabolism compared with two species of pulsating scyphozoan jellyfish, Aurelia aurita and Pelagia noctiluca. Protein (P), lipid (L), carbohydrate (K), and derived energy content (Ec), provided information on the biochemical composition of these species and their relevance as prey. Physiological respiration (R) from oxygen consumption. As well as potential respiration (Φ) from the electron transport system (ETS) activity and the derived respiratory carbon demand (RCD) and heterotrophic energy transformation (HET), allow the comparison of the impact of these two types of propulsion on the metabolism, along with the impact of these organisms as predators. In this study it was found that these hydrozoans depicted a different biochemical composition relative to other gelatinous zooplankton. Lower water content at around 90% was observed, while WM-specific P, L, K, and Ec were higher, showcasing new aspects of these species as prey. The lower R/P in P. physalis and V. velella (1.8 ± 0.7 and 2.9 ± 1.1 μL O2 h–1 mg Prot–1, respectively) and the low R/Φ, around 0.1, indicate lower respiration in wind-driven propulsion compared to pulsation-driven propulsion. Additionally, these results encourage the use and research on enzymatic techniques that are particularly useful for gelatinous research, and the calculation of RCD and HET helps in understanding the physiology and role played by the organisms as predators from carbon and energy perspectives.
... Some authors have demonstrated the success of a mutualistic interaction with C. andromeda under stressful environmental conditions in shallow waters, i.e., high temperatures, high levels of irradiation, eutrophic conditions, and changes in salinity [33]. These life history traits also permitted this species to become an invader in the Mediterranean Sea, where, being one of the earliest Lessepsian migrants, C. andromeda has spread, reaching the western Mar Menor in Spain, being randomly spotted in the Levant Sea, Aegean Sea, and Strait of Sicily [6,[34][35][36]. ...
Simple Summary
Alien species are an important cause of biodiversity loss and changes to ecosystems. Harbors are hotspots for the introduction of these species, and, usually, the impacts and pathways of invasion of the host populations are poorly known. Since 2014, an alien jellyfish, Cassiopea andromeda, coming from the Red Sea, has invaded a Mediterranean touristic harbor and established a population there. In this study, the distribution and trophic behavior of C. andromeda were investigated to improve knowledge on this species within the Mediterranean. The preliminary results highlight and confirm that C. andromeda is a perfect invader thanks to its nutritional strategy and capacity to adapt to heavily anthropized areas. Therefore, its potential impact on the local biodiversity and thus on the ecosystem’s structure and functioning is worth considering.
Abstract
Harbors are hotspots for the introduction of alien species, and, usually, investigations on their host populations help fill the knowledge gap in their pathways of invasion and in their impacts on marine biodiversity and ecosystems. In 2014, the upside-down alien jellyfish Cassiopea andromeda invaded a Mediterranean touristic harbor (“Cala”), and its abundance has since increased over time. In the present study, the distribution and trophic behavior of C. andromeda in Cala were investigated for the years 2017–2018 through visual sampling, and GIS-based statistical and stable isotope analyses. Since Cala is a hard-to-reach area (with many anchor cables and boats), Megabenthos Underwater Video was used to count the number and estimate the size of jellyfishes. The variations in size throughout the study period suggest that the population of C. andromeda is quite established in Cala at depths lower than 7.5 m. The ranges of the environmental parameters recorded (temperature, salinity, and transparency) were consistent with the ideal conditions for maintaining a Cassiopea population, but they did not seem to influence aggregation. Additionally, the carbon and nitrogen isotopic signatures studied highlight the mixotrophic behavior of this species. These preliminary results confirm the capacity of C. andromeda to live and reproduce in heavily anthropized areas.
... The start and end of transects were marked with buoys and 1 m PVC pipe for scale. The transects did not go deeper than 60 cm because Cassiopea mostly occur in shallow water environments and can reliably be detected at this depth [17,29,31,40]. A secchi disc measurement in the middle of each site was used to assess relative water clarity and visibility. ...
Upside-down jellyfish (Cassiopea sp.) are mostly sedentary, benthic jellyfish that have invaded estuarine ecosystems around the world. Monitoring the spread of this invasive jellyfish must contend with high spatial and temporal variability in abundance of individuals, especially around their invasion front. Here, we evaluated the utility of drones to survey invasive Cassiopea in a coastal lake on the east coast of Australia. To assess the efficacy of a drone-based methodology, we compared the densities and counts of Cassiopea from drone observations to conventional boat-based observations and evaluated cost and time efficiency of these methods. We showed that there was no significant difference in Cassiopea density measured by drones compared to boat-based methods along the same transects. However, abundance estimates of Cassiopea derived from scaling-up transect densities were over-inflated by 319% for drones and 178% for boats, compared to drone-based counts of the whole site. Although conventional boat-based survey techniques were cost-efficient in the short-term, we recommend doing whole-of-site counts using drones. This is because it provides a time-saving and precise technique for long-term monitoring of the spatio-temporally dynamic invasion front of Cassiopea in coastal lakes and other sheltered marine habitats with relatively clear water.
... S. roscoffensis, whose entire life-cycle can be completed in the lab, serves as a marine model system for photosymbiosis and for the study of physiological processes supported by the tripartite association between the host, microalgae and microbiome such as the production of dimethylsulfoniopropionate (DMSP) (Arboleda et al., 2018). Cassiopea sp. and Exaiptasia sp. are the equivalent of "laboratory rats" for cnidarian research, especially the cnidarian-zooxanthellae symbiosis (Lampert, 2016;Rädecker et al., 2018) and, more recently, as models with the potential of providing a basic functional understanding of cnidarian microbiomes (Herrera et al., 2017). ...
In the past 20 years, a new concept has slowly emerged and expanded to various domains of marine biology research: the holobiont. A holobiont describes the consortium formed by a eukaryotic host and its associated microorganisms including bacteria, archaea, protists, microalgae, fungi, and viruses. From coral reefs to the deep-sea, symbiotic relationships and host–microbiome interactions are omnipresent and central to the health of marine ecosystems. Studying marine organisms under the light of the holobiont is a new paradigm that impacts many aspects of marine sciences. This approach is an innovative way of understanding the complex functioning of marine organisms, their evolution, their ecological roles within their ecosystems, and their adaptation to face environmental changes. This review offers a broad insight into key concepts of holobiont studies and into the current knowledge of marine model holobionts. Firstly, the history of the holobiont concept and the expansion of its use from evolutionary sciences to other fields of marine biology will be discussed. Then, the ecology and physiology of marine holobionts will be investigated through the examples of corals and sponges. We will discuss the impacts of environmental change on organisms at the holobiont level and how microbiomes contribute to the resilience and/or vulnerability of their host in the face of environmental stressors. Finally, we will conclude with the development of new technologies, holistic approaches, and future prospects for conservation biology surrounding marine holobionts.
... Here, changes in light penetration were reproduced in laboratory experiments to assess the physiological plasticity of the photosynthetic machinery of Cassiopea jellyfish in response to a simulated transition from a harbor-typical high turbidity condition to a meso-oligotrophic, coastal open water condition. In addition to its eurythermal tolerance [68,69], our results indicate that Cassiopea autotrophic system is highly adaptive. Harbors and other anthropogenic sheltered areas can therefore act as initial settling terminals for upside-down early founder jellyfishes; also, it is foreseeable that the progressive northward displacement of the 15˚isotherm will be paralleled by Cassiopea population spillover in the surrounding natural habitats of the Western Mediterranean Sea, as it already happened into the Levantine basin [47,49]. ...
Ecological profiling of non-native species is essential to predict their dispersal and invasiveness potential across different areas of the world. Cassiopea is a monophyletic taxonomic group of scyphozoan mixotrophic jellyfish including C. andromeda, a recent colonizer of sheltered, shallow-water habitats of the Mediterranean Sea, such as harbors and other light-limited, eutrophic coastal habitats. To assess the ecophysiological plasticity of Cassiopea jellyfish and their potential to spread across the Mare Nostrum by secondary introductions, we investigated rapid photosynthetic responses of jellyfish to irradiance transitions—from reduced to increased irradiance conditions (as paradigm of transition from harbors to coastal, meso/oligotrophic habitats). Laboratory incubation experiments were carried out to compare oxygen fluxes and photobiological variables in Cassiopea sp. immature specimens pre-acclimated to low irradiance (PAR = 200 μmol photons m⁻² s⁻¹) and specimens rapidly exposed to higher irradiance levels (PAR = 500 μmol photons m⁻² s⁻¹). Comparable photosynthetic potential and high photosynthetic rates were measured at both irradiance values, as also shown by the rapid light curves. No significant differences were observed in terms of symbiont abundance between control and treated specimens. However, jellyfish kept at the low irradiance showed a higher content in chlorophyll a and c (0.76±0.51SD vs 0.46±0.13SD mg g⁻¹ AFDW) and a higher Ci (amount of chlorophyll per cell) compared to jellyfish exposed to higher irradiance levels. The ratio between gross photosynthesis and respiration (P:R) was >1, indicating a significant input from the autotrophic metabolism. Cassiopea sp. specimens showed high photosynthetic performances, at both low and high irradiance, demonstrating high potential to adapt to sudden changes in light exposure. Such photosynthetic plasticity, combined with Cassiopea eurythermal tolerance and mixotrophic behavior, jointly suggest the upside-down jellyfish as a potentially successful invader in the scenario of a warming Mediterranean Sea.
... Of them, jellyfish with subumbrellar muscles in featherlike arcs belong to a single-family Cassiopeidae that is also a monotypic taxon comprising of the genus Cassiopea (Kramp 1961). Ten species have been classified into the genus Cassiopea (Kramp 1961;Hummelinck 1968;Thiel 1975;WoRMS Editorial Board 2020); and they show different colour morphs due to the colour producing dinoflagellate algae (zooxanthellae) that live within them symbiotically for photosynthesis (Rahat and Adar 1980;Lampert et al. 2012;Lampert 2016 The tropical Indo-Pacific region is a biodiversity hotspot for these cassiopeids (Schembri et al. 2010), which most often occur in shallow bays, intertidal sands, mangrove mudflats and lagoons (Browne 1916). Cassiopea andromeda (Forskål, 1775) is a common upsidedown jellyfish originally reported from the Red Sea, but now it has been reported as an invasive or alien species around the world (Galil et al. 1990;Zenetos et al. 2005Zenetos et al. , 2011Çevik et al. 2006;Özgür and Öztürk 2008;Schembri et al. 2010;Katsanevakis 2011;Gülşahin and Tarkan 2012), therefore, it referred as ecologically important species by concerning its invasive distribution (Heins et al. 2015). ...
The circumtropical upside-down jellyfish Cassiopea andromeda is native to the Indian region, but no scientific documentations are confirming its presence in Sri Lankan waters. Hence in this paper, the occurrence of C. andromeda in Sri Lankan waters is reported for the first time. Species identification was based on several specimens collected from shallow waters of north and east coasts of the country in 2017. The C. andromeda found from Sri Lanka is a mild stinger and so far there are no reports on severe health issues cause to fishers and tourists. Also, this species was identified as a potential ornamental species due to its gorgeous appearance with very high colour variation.
... In the last few years, research on these gelatinous species has increased and Cassiopea has been considered a model species in studying symbiotic relationships due to the ease of culturing and maintaining polyps and medusae in the laboratory, but also because the Cassiopea/Symbiodinium interaction is a clear example of a successful cooperation under stressful environmental conditions (shallow waters, high temperatures, high levels of irradiation and potentially large changes in salinity) and therefore it is also interesting in a climate change context (Lampert, 2016). Moreover, Cassiopea spp. ...
The upside-down jellyfish Cassiopea is a benthic scyphozoan, considered a non-indigenous invasive species in the Mediterranean, forming large blooms in eutrophic areas. Taxonomy of the genus Cassiopea is extremely difficult because morphological/meristic characters used are variable within the same species, overlapping among different species, and cryptic species have been identified by molecular markers; nine Cassiopea species are recognized on the basis of molecular study. Mediterranean records of Cassiopea have been ascribed to andromeda species on the basis of a hypothesized invasion pathway from the Suez Canal. In the current study, an analysis of the main morphological characters of the sampled Cassiopea jellyfish from Palermo (Tyrrhenian Sea) was carried out and subsequently, molecular analyses were performed by using COI barcode in order to identify the species. Molecular data were compared with published information in GenBank. Morphological characters were highly variable, but molecular analyses confirmed that Mediterranean Cassiopea specimens belong to andromeda species. Moreover, high values of sequence divergence were found between Mediterranean Cassiopea and the other C. andromeda from the Red Sea, Hawaii and Florida. These results lead to a discussion of possible explanations linked to life history features of the species. Two different explanations are proposed; the first is that Mediterranean C. andromeda , finding a suitable ecological niche good for colonization and proliferation, could have been isolated in Palermo Harbour. The second considers the possibility of multiple introduction events by human transport as demonstrated for other non-indigenous jellyfish; in this case Cassiopea genetic differences increased in the invaded area.
... Upside-down jellyfish, Cassiopea spp., are host to S. microadriaticum, and require the presence of these symbionts to complete their life cycle (Hofmann, Neumann, & Henne, 1978;Mellas, McIlroy, Fitt, & Coffroth, 2014;Pitt, Welsh, & Condon, 2009). These zooxanthellae may be absorbed by the jellyfish from the surrounding water, or may be acquired in the process of feeding (Fitt, 1984;Fitt & Costley, 1998;Lampert, 2016 Cassiopea spp. are globally distributed in tropical coastal waters such as mangroves and lagoons (Holland, Dawson, Crow, & Hofmann, 2004). ...
Ocean acidification is the decline in seawater pH that results from the absorption of atmospheric carbon dioxide (CO2). Decreased pH has negative effects on survivability, growth, and development in many marine calcifiers, potentially resulting in reduced coral species richness. This reduction in richness could open new niche space, allowing the spread of invasive species, such as the upside‐down jellyfish (Cassiopea spp.). Like corals, this jellyfish forms symbiotic relationships with zooxanthellae, photosynthetic dinoflagellates. This study focused on the effect of seawater acidification in Cassiopea spp. We monitored zooxanthellae density and two measures of health (bell diameter and volume) in individuals of Cassiopea sp. at three pH levels chosen to mimic different open‐ocean average conditions: 8.2, representing pre‐industrial revolution conditions; and 7.9 and 7.6, representing predicted declines in pH in the next century. Zooxanthellae density and health of the jellyfish were measured twice—prior to experimental manipulations and after four weeks of exposure to experimental pHs—in three consecutive trials. The effects of pH and Trial on proportional change in jellyfish attributes were analyzed using generalized linear mixed models. We found no significant effects of either factor. These results indicate that decreasing seawater pH has no apparent negative effect on zooxanthellae density or health in Cassiopea, which suggests that these jellyfish may be relatively insensitive to the impacts of ocean acidification, heightening its potential as an invasive species.
... The stalked jellyfish C. cruxmelitensis has been the recent subject of detailed anatomic [20] and biodiversity studies [27]. The upside-down jellyfish C. xamachana is an established model for understanding cnidarian-dinoflagellate endosymbiosis [66] and, with its ease of culturing and tractability in the laboratory setting, is poised as a model system for evolutionary developmental biology research and other laboratory-based studies [67]. ...
Background
Anthozoa, Endocnidozoa, and Medusozoa are the 3 major clades of Cnidaria. Medusozoa is further divided into 4 clades, Hydrozoa, Staurozoa, Cubozoa, and Scyphozoa—the latter 3 lineages make up the clade Acraspeda. Acraspeda encompasses extraordinary diversity in terms of life history, numerous nuisance species, taxa with complex eyes rivaling other animals, and some of the most venomous organisms on the planet. Genomes have recently become available within Scyphozoa and Cubozoa, but there are currently no published genomes within Staurozoa and Cubozoa.
Findings
Here we present 3 new draft genomes of Calvadosia cruxmelitensis (Staurozoa), Alatina alata (Cubozoa), and Cassiopea xamachana (Scyphozoa) for which we provide a preliminary orthology analysis that includes an inventory of their respective venom-related genes. Additionally, we identify synteny between POU and Hox genes that had previously been reported in a hydrozoan, suggesting this linkage is highly conserved, possibly dating back to at least the last common ancestor of Medusozoa, yet likely independent of vertebrate POU-Hox linkages.
Conclusions
These draft genomes provide a valuable resource for studying the evolutionary history and biology of these extraordinary animals, and for identifying genomic features underlying venom, vision, and life history traits in Acraspeda.
... Sister to Anthozoa is the clade Medusozoa which includes Hydrozoa, Scyphozoa, Staurozoa and Cubozoa. While the latter two taxa are not reported to be symbiotic, some members of the Scyphozoa, the upside-down jellyfish of the genus Cassiopea, harbour Symbiodinium (Thornhill et al., 2006;Lampert, 2016). In Hydrozoa, the situation is more complex: the H. viridissima group (also referred to as green Hydra), the H. vulgaris group and the H. oligactis group are symbiotic with chlorophyte algae of the genus Chlorella or Chlorococcum (Matthias, Frederike & Thomas, 2003;Bosch, 2012;Kawaida et al., 2013), but only in H. viridissima is the symbiosis stable (Kawaida et al., 2013;Ishikawa et al., 2016). ...
Mutualistic symbioses are common throughout the animal kingdom. Rather unusual is a form of symbiosis, photosymbiosis, where animals are symbiotic with photoautotrophic organisms. Photosymbiosis is found among sponges, cnidarians, flatworms, molluscs, ascidians and even some amphibians. Generally the animal host harbours a phototrophic partner, usually a cyanobacteria or a unicellular alga. An exception to this rule is found in some sea slugs, which only retain the chloroplasts of the algal food source and maintain them photosynthetically active in their own cytosol – a phenomenon called ‘functional kleptoplasty’. Research has focused largely on the biodiversity of photosymbiotic species across a range of taxa. However, many questions with regard to the evolution of the ability to establish and maintain a photosymbiosis are still unanswered. To date, attempts to understand genome adaptations which could potentially lead to the evolution of photosymbioses have only been performed in cnidarians. This knowledge gap for other systems is mainly due to a lack of genetic information, both for non‐symbiotic and symbiotic species. Considering non‐photosymbiotic species is, however, important to understand the factors that make symbiotic species so unique. Herein we provide an overview of the diversity of photosymbioses across the animal kingdom and discuss potential scenarios for the evolution of this association in different lineages. We stress that the evolution of photosymbiosis is probably based on genome adaptations, which (i) lead to recognition of the symbiont to establish the symbiosis, and (ii) are needed to maintain the symbiosis. We hope to stimulate research involving sequencing the genomes of various key taxa to increase the genomic resources needed to understand the most fundamental question: how have animals evolved the ability to establish and maintain a photosymbiosis?
The upside-down jellyfish holobiont, Cassiopea xamachana, is a useful model system for tri-partite interactions between the cnidarian host, the photosymbiont, and the bacterial microbiome. While the interaction between the host and photosymbiont has been well studied, less is understood of the associated bacterial community. To date, the bacterial microbiome of wild C. xamachana has remained largely uncharacterized. Thus, wild medusae (n=6) and larvae (n=3) were collected from two sites in the Florida Keys. Bacterial community composition was characterized via amplicon sequencing of the 16S rRNA gene V4 region. The medusa bacterial community was dominated by members of the Alphaproteobacteria and Gammaproteobacteria, while Planctomycetota, Actinomycetota, Bacteroidota, and Bacillota were also present, among others. Community composition was consistent between locations and across medusa structures (oral arm, bell, and gonad). The larval bacterial community clustered apart from the medusa community in beta diversity analysis and was characterized by the presence of several Pseudomonadota taxa that were not present in the medusa, including the Alteromonas, Pseudoalteromonas, and Thalassobius genera. A bacterial isolate library encompassing much of the amplicon sequencing diversity was also developed and tested via metabolic assays in a separate culture-dependent analysis of isolates from medusa bells, oral arms, and laplets. Most characteristics were not correlated with host sex or medusa structure, but gelatinase production was more common in laplet isolates, while lactose fermentation was more common in female oral arm isolates. The Endozoicomonas genus was dominant in both amplicon sequencing and in our isolate library, and was equally prevalent across all medusa structures and in both sexes. Understanding the bacterial component of the C. xamachana holobiont will allow us to further develop this important model cnidarian holobiont.
The jellyfish Cassiopea largely cover their carbon demand via photosynthates produced by microalgal endosymbionts, but how holobiont morphology and tissue optical properties affect the light microclimate and symbiont photosynthesis in Cassiopea remain unexplored. Here, we use optical coherence tomography (OCT) to study the morphology of Cassiopea medusae at high spatial resolution. We include detailed 3D reconstructions of external micromorphology, and show the spatial distribution of endosymbionts and white granules in the bell tissue. Furthermore, we use OCT data to extract inherent optical properties from light-scattering white granules in Cassiopea, and show that granules enhance local light-availability for symbionts in close proximity. Individual granules had a scattering coefficient of µs = 200–300 cm⁻¹, and scattering anisotropy factor of g = 0.7, while large tissue-regions filled with white granules had a lower µs = 40–100 cm⁻¹, and g = 0.8–0.9. We combined OCT information with isotopic labelling experiments to investigate the effect of enhanced light-availability in whitish tissue regions. Endosymbionts located in whitish tissue exhibited significantly higher carbon fixation compared to symbionts in anastomosing tissue (i.e. tissue without light-scattering white granules). Our findings support previous suggestions that white granules in Cassiopea play an important role in the host modulation of the light-microenvironment.
The upside-down jellyfish Cassiopea engages in symbiosis with photosynthetic microalgae that facilitate uptake and recycling of inorganic nutrients. By contrast to most other symbiotic cnidarians, algal endosymbionts in Cassiopea are not restricted to the gastroderm but are found in amoebocyte cells within the mesoglea. While symbiont-bearing amoebocytes are highly abundant, their role in nutrient uptake and cycling in Cassiopea remains unknown. By combining isotopic labelling experiments with correlated scanning electron microscopy, and Nano-scale secondary ion mass spectrometry (NanoSIMS) imaging, we quantified the anabolic assimilation of inorganic carbon and nitrogen at the subcellular level in juvenile Cassiopea medusae bell tissue. Amoebocytes were clustered near the sub-umbrella epidermis and facilitated efficient assimilation of inorganic nutrients. Photosynthetically fixed carbon was efficiently translocated between endosymbionts, amoebocytes and host epidermis at rates similar to or exceeding those observed in corals. The Cassiopea holobionts efficiently assimilated ammonium, while no nitrate assimilation was detected, possibly reflecting adaptation to highly dynamic environmental conditions of their natural habitat. The motile amoebocytes allow Cassiopea medusae to distribute their endosymbiont population to optimize access to light and nutrients, and transport nutrition between tissue areas. Amoebocytes thus play a vital role for the assimilation and translocation of nutrients in Cassiopea , providing an interesting new model for studies of metabolic interactions in photosymbiotic marine organisms.
Introduction
The potential efficacy of selected plant extracts to counteract the dermal toxicity of jellyfish envenomation was investigated using an in vitro cell culture model.
Methods
We studied plant extracts from Carica papaya, Ananas comosus, and Bouvardia ternifolia, known for their antivenom properties, in pairwise combinations with tissue homogenates of the jellyfish Pelagia noctiluca, Phyllorhiza punctata, and Cassiopea andromeda, to evaluate modulations of jellyfish cytotoxic effects. L929 mouse fibroblasts were incubated with pairwise jellyfish/plant extract combinations and examined by MTT assay (3-[4,5-dimethylthiazol-2-yl]-2,5-diphenyltetrazolium bromide).
Results
C papaya and A comosus significantly lowered the cytotoxicity of P noctiluca and P punctata but induced a slight worsening of C andromeda cytotoxicity. Conversely, B ternifolia was protective against P punctata, ineffective against P noctiluca, and worsened C andromeda cytotoxicity.
Conclusions
Data showed species-specific and contrasting effects of plant extracts, suggesting that those containing protease activities, namely A comosus and C papaya, are more effective in lowering the cytotoxicity of jellyfish venom containing toxic peptidic factors such as phospholipase A. However, all examined plants require further investigation in vivo to evaluate their ability to counteract jellyfish injury to the skin.
The sea anemone Entacmaea medusivora (Actiniaria, Anthozoa) commonly feeds on the golden jellyfish Mastigias papua (Rhizostomeae, Scyphozoa) which harbours endosymbiotic dinoflagellate of the genus Cladocopium (Symbiodiniaceae). In this study, we monitored the photosynthetic activity of the endosymbiotic microalgae while their host jellyfish were ingested and digested by starved medusivorous anemones. By analyzing the photosynthetic yield of photosystem II, we observed that Cladocopium cells remain photosynthetically competent during the whole digestion process, thus confirming the exceptional resistance of Symbiodiniaceae to digestive enzymes. In the gastric cavity of E. medusivora, Cladocopium cells release oxygen, which could broadly stimulate the gastric microbiotic flora of the sea anemone. Ultimately, E. medusivora is not able to retain Cladocopium cells more than few days and physiologically-unaltered cells are therefore expelled in faecal pellets. The potential contribution of E. medusivora to maintain a reservoir of Cladocopium symbionts and its role in the life cycle of M. papua is discussed.
The mutualistic relationship between dinoflagellates in the genus Symbiodinium microadriaticum and animals in the phylum Cnidaria, specifically corals, make up one of the most well-known symbioses in the marine environment. The nature of the relationship is such that these symbiotic algae provide products of photosynthesis to their cnidarian hosts, while the algae are afforded refuge within the endodermal cells of the host. Use of the model system Cassiopea xamachana (a.k.a. the ‘upside down jellyfish’), a scyphozoan that can be reared throughout its entire life cycle in a laboratory setting, allowed for the study of the cnidarian-algal symbiosis without many of the constraints involved when working with corals and other cnidarians. The aposymbiotic polyp stage of C. xamachana was used in this study to visualize the acquisition of algal cells by endodermal cells of host animals, a requisite phenomenon for the transition to a free living medusae (strobilation). Polyps harboring algae from environmental sources prior to experimentation were subjected to high temperatures to initiate the expulsion of algae and to obtain polyps that were completely free of symbionts (aposymbiotic); bleaching was confirmed with high resolution confocal microscopy. Aposymbiotic polyps were subsequently introduced to low numbers of Symbiodinium, and the intrinsic growth rate of algae calculated based on count data generated at 7-day intervals. Symbiodinium used for reintroduction in experimental trials were obtained from three sources: (1) commercially cultured algal cells (type A194), (2) algae that had been expelled from their host tissues following heat-induced bleaching in the laboratory, and (3) algae freshly isolated from an adult medusa. These three sources of algal cells were used to represent the possible reservoirs from which bleached animals might replenish their symbiont population following a bleaching event. Symbiodinium cells were acquired by C. xamachana polyps in all three treatment groups, although cultured Symbiodinium A194 exhibited the slowest mean intrinsic growth rate (0.054 d⁻¹) once they were housed within endodermal cells of their host. Mean time to strobilation was accordingly slow (>120 days) for those polyps harboring type A194 symbionts. In fact, polyps harboring other sourced Symbiodinium strobilated in <70 days on average. Though it is known that strobilation does not occur without the acquisition of symbionts during the polyp stage, the results provided in this study demonstrate clearly that the number of symbionts at the time of strobilation can vary greatly. This variation in symbiont number just prior to strobilation, substantiates previous documented evidence that strobilation is not only stimulated by acquisition of Symbiodinium, but by other triggers as well. Our methods allow quantitative methods to be used to discover additional components involved in the establishment of successful symbiosis between these species.
Impairment of the photosynthetic machinery of the algal endosymbiont ("zooxanthellae") is the proximal driver of the thermal breakdown of the coral-algae symbiosis ("coral bleaching"). Yet, the initial site of damage, and early dynamics of the impairment are still not well resolved. In this perspective essay, I consider further a recent hypothesis which proposes an energetic disruption to the carbon-concentrating mechanisms (CCMs) of the coral host, and the resultant onset of CO2-limitation within the photosynthetic "dark reactions" as a unifying cellular mechanism. The hypothesis identifies the enhanced retention of photosynthetic carbon for zooxanthellae (re)growth following an initial irradiance-driven expulsion event as a strong contributing cause of the energetic disruption. If true, then it implies that the onset of the bleaching syndrome and setting of upper thermal bleaching limits are emergent attributes of the coral symbiosis that are ultimately underpinned by the characteristic growth profile of the intracellular zooxanthellae; which is known to depend not just on temperature, but also external (seawater) nutrient availability and zooxanthellae genotype. Here, I review this proposed bleaching linkage at a variety of observational scales, and find it to be parsimonious with the available evidence. Future experiments are suggested that can more formally test the linkage. If correct, the new cellular model delivers a valuable new perspective to consider the future prospects of the coral symbiosis in an era of rapid environmental change, including: (i) the underpinning mechanics (and biological significance) of observed changes in resident zooxanthellae genotypes, and (ii) the now crucial importance of reef water quality in co-determining thermal bleaching resistance.
The symbiotic dinoflagellates (genus Symbiodinium) inhabiting coral endodermal tissues are well known for their role as keystone symbiotic partners, providing corals with enormous amounts of energy acquired via photosynthesis and the absorption of dissolved nutrients. In the past few decades, corals reefs worldwide have been increasingly affected by coral bleaching (i.e., the breakdown of the symbiosis between corals and their dinoflagellate symbionts), which carries important socio-economic implications. Consequently, the number of studies focusing on the molecular and cellular processes underlying this biological phenomenon has grown rapidly, and symbiosis is now widely recognized as a major topic in coral biology. However, obtaining a clear image of the interplay between the environment and this mutualistic symbiosis remains challenging. Here, we review the potential of recent technological advances in molecular biology and approaches using stable isotopes to fill critical knowledge gaps regarding coral symbiotic function. Finally, we emphasize that the largest opportunity to achieve the full potential in this field arises from the integration of these technological advances.
Coral reef ecosystems thrive in tropical oligotrophic oceans because of the relationship between corals and endosymbiotic dinoflagellate algae called Symbiodinium. Symbiodinium convert sunlight and carbon dioxide into organic carbon and oxygen to fuel coral growth and calcification, creating habitat for these diverse and productive ecosystems. Light is thus a key regulating factor shaping the productivity, physiology, and ecology of the coral holobiont. Similar to all oxygenic photoautotrophs, Symbiodinium must safely harvest sunlight for photosynthesis and dissipate excess energy to prevent oxidative stress. Oxidative stress is caused by environmental stressors such as those associated with global climate change, and ultimately leads to breakdown of the coral–algal symbiosis known as coral bleaching. Recently, large-scale coral bleaching events have become pervasive and frequent threatening and endangering coral reefs. Because the coral–algal symbiosis is the biological engine producing the reef, the future of coral reef ecosystems depends on the ecophysiology of the symbiosis. This review examines the photobiology of the coral–algal symbiosis with particular focus on the photophysiological responses and timescales of corals and Symbiodinium. Additionally, this review summarizes the light environment and its dynamics, the vulnerability of the symbiosis to oxidative stress, the abiotic and biotic factors influencing photosynthesis, the diversity of the coral–algal symbiosis, and recent advances in the field. Studies integrating physiology with the developing “omics” fields will provide new insights into the coral–algal symbiosis. Greater physiological and ecological understanding of the coral–algal symbiosis is needed for protection and conservation of coral reefs.
Understanding the ecology and evolution of the cnidarian-algal symbiosis is of major scientific interest as it is sensitive to temperature and strong light and may therefore be susceptible to climate change. The stability of this mutualism is often mediated by host color pigments that influence photosynthetic activity in symbiotic dinoflagellates either by providing the photosystem with irradiance of suitable wavelength or by protecting it from much too much and potentially damaging light. Like scleractinian corals, the upside-down jellyfish, Cassiopea andromeda, relies heavily on the nutrients provided by its symbionts of the dinoflagellate genus Symbiodinium. It occurs in several conspicuously different color morphs and is found in habitats with high levels of irradiation. We tested whether the color morphs of Cassiopea were correlated with the Symbiodinium distribution in the host and whether host color was associated with different clades of Symbiodinium. We found that the presence of color pigment did not correlate with the distribution of Symbiodinium in the host. Symbiodinium was found in both the colored tentacles of the jellyfish and the colorless feeding tentacles. At least six different color morphs co-occurred in the very shallow waters of the Red Sea, but they all hosted a single Symbiodinium clade (clade A1). Therefore, no correlation of host color morph and Symbiodinium clade could be found. Photoaccumulative or photoprotective functions of host pigments, as proposed for some scleractinian corals, thus seem unlikely in the colored tentacles (vesicles) of the upside-down jellyfish Cassiopea andromeda.
Two populations of the conspicuous, semi-sessile medusae of the rhizostome genus Cassiopea, both morphologically similar to Cassiopea andromeda from the Red Sea and Indopacific, were recently studied on Oahu (Hawai'i), one from a sheltered saltwater pond (the Hilton Lagoon) next to Ala Wai Harbor, Honolulu, and the second from the canals of a fish farm near Kahuku on NE Oahu. Gonad differentiation, checked in 1998, and again in 1999 and 2000, was unexpectedly different in medusae from these two locations. Contrary to all earlier reports and personal observations of strict gonochorism in C. andromeda, the majority of the Hilton Lagoon medusae collected in 1998 were hermaphroditic with female and male parts intermingling in the gonads. This is an exceptional case in scyphozoans. However, this hermaphroditic condition, which was observed again in 1999, was not stable over time. All six medusae taken from the same lagoon in 2000 were distinctly gonochoristic; four were males, and two were females brooding egg masses on the oral disk. Planula larvae hatching in the laboratory were successfully reared to the scyphopolyp stage. By contrast, medusae sampled from the population were all males in 1998, 1999, and 2000. Polyps were found abundantly on dark, deteriorating leaves of the Red Mangrove, occasionally on other plant remnants, and on discarded plastic materials in the canals. The polyps propagated asexually both by strobilation of ephyrae and by production of motile, larva-like buds that settled to form additional polyps. We speculate on a clonal origin of this male population. Asexually formed propagules were induced to form polyps by exposure to either the peptide Z-GPGGPA or biogenic substrata as has been shown before in other Cassiopea species. The serine/threonine protein phosphatase inhibitor cantharidin stimulated bud development too, but interfered strongly with pattern formation, polarity, and the sequence and timing of morphogenetic events. It did not induce typical bud-to-polyp metamorphosis.
The association between the symbiont Symbiodinium microadriaticum (zooxanthellae) and its host jellyfish, Cassiopea xamachana, was investigated as a function of jellyfish size and season. Symbiont cell diameter and volume were higher during January than September. Although zooxanthella-specific chlorophyll was independent of jellyfish size, both chlorophyll a and c were higher during January. Regardless of season, algal density and jellyfish size were inversely related. The diel mitotic index (MI) of zooxanthellae was phased, with a peak of 0.25% occurring between 09:00 and 12:00 h. September photosynthetic rates were always higher than January rates and reflected the seasonal light and temperature regimes at the latitude of the Florida Keys (USA). Photosynthesis, when normalized to either zooxanthella density or protein, displayed an inverse relationship with jellyfish size. Medusan respiration rates also showed an inverse relationship with jellyfish size, with September metabolism being higher than that of January. The carbon budgets calculated for these medusae indicate that the carbon photosynthetically fixed by the zooxanthellae, and subsequently translocated to the host, is capable of satisfying about 169% of the host's metabolic demand (CZAR) and is independent of both jellyfish size and season. These seasonally influenced physiological effects underscore the necessity for seasonal examinations of algal-cnidarian symbioses in order to understand the photophysiology of the association on an annual basis.
The dinoflagellate photosymbiont Symbiodinium plays a fundamental role in defining the physiological tolerances of coral holobionts, but little is known about the dynamics of these endosymbiotic populations on coral reefs. Sparse data indicate that Symbiodinium populations show limited spatial connectivity; however, no studies have investigated temporal dynamics for in hospite Symbiodinium populations following significant mortality and recruitment events in coral populations. We investigated the combined influences of spatial isolation and disturbance on the population dynamics of the generalist Symbiodinium type C2 (ITS1 rDNA) hosted by the scleractinian coral Acropora millepora in the central Great Barrier Reef. Using eight microsatellite markers, we genotyped Symbiodinium in a total of 401 coral colonies, which were sampled from seven sites across a 12-year period including during flood plume-induced coral bleaching. Genetic differentiation of Symbiodinium was greatest within sites, explaining 70-86% of the total genetic variation. An additional 9-27% of variation was explained by significant differentiation of populations among sites separated by 0.4-13 km, which is consistent with low levels of dispersal via water movement and historical disturbance regimes. Sampling year accounted for 6-7% of total genetic variation and was related to significant coral mortality following severe bleaching in 1998 and a cyclone in 2006. Only 3% of the total genetic variation was related to coral bleaching status, reflecting generally small (8%) reductions in allelic diversity within bleached corals. This reduction probably reflected a loss of genotypes in hospite during bleaching, although no site-wide changes in genetic diversity were observed. Combined, our results indicate the importance of disturbance regimes acting together with limited oceanographic transport to determine the genetic composition of Symbiodinium types within reefs.
Coral reefs face multiple anthropogenic threats, from pollution and overfishing to the dual effects of greenhouse gas emissions: rising sea temperature and ocean acidification [1]. While the abundance of coral has declined in recent decades [2, 3], the implications for humanity are difficult to quantify because they depend on ecosystem function rather than the corals themselves. Most reef functions and ecosystem services are founded on the ability of reefs to maintain their three-dimensional structure through net carbonate accumulation [4]. Coral growth only constitutes part of a reef's carbonate budget; bioerosion processes are influential in determining the balance between net structural growth and disintegration [5, 6]. Here, we combine ecological models with carbonate budgets and drive the dynamics of Caribbean reefs with the latest generation of climate models. Budget reconstructions using documented ecological perturbations drive shallow (6-10 m) Caribbean forereefs toward an increasingly fragile carbonate balance. We then projected carbonate budgets toward 2080 and contrasted the benefits of local conservation and global action on climate change. Local management of fisheries (specifically, no-take marine reserves) and the watershed can delay reef loss by at least a decade under "business-as-usual" rises in greenhouse gas emissions. However, local action must be combined with a low-carbon economy to prevent degradation of reef structures and associated ecosystem services.
The total daily flux of photosynthetically fixed carbon in light- and shade-adapted phenotypes of the symbiotic coral, Stylophora pistillata, was quantified. Light adapted corals fixed four times as much carbon and respired twice as much as shade corals. Specific growth rates of zooxanthellae in situ were estimated from average daily mitotic indices and from ammonium uptake rates (nitrate uptake or nitrate reductase activity could not be demonstrated). Specific growth rates were very low, demonstrating that of the total net carbon fixed daily, only a small fraction (less than 5%) goes into zooxanthellae cell growth. The balance of the net fixed carbon (more than 95%) is translocated to the host. New and conventional methods of measuring total daily translocation were compared. The `growth rate' method, which does not employ 14C, emerged as superior to the conventional in vitro and in vivo methods. The contribution of translocated carbon to animal maintenance respiration (CZAR) was 143% in light corals and 58% in shade corals. Thus, translocation in the former could supply not only the total daily carbon needed for respiration but also a fraction of the carbon needed for growth. Whereas light-adapted corals released only 6%, shade-adapted corals released almost half of their total fixed carbon as dissolved or particulate organic material. This much higher throughput of organic carbon may possibly benefit the heterotrophic microbial community in shade environments.
Coral reefs thrive in part because of the symbiotic partnership between corals and Symbiodinium. While this partnership is one of the keys to the success of coral reef ecosystems, surprisingly little is known about many aspects of coral symbiosis, in particular the estab-lishment and development of symbiosis in host species that acquire symbionts anew in each generation. More specifi-cally, the point at which symbiosis is established (i.e., larva vs. juvenile) remains uncertain, as does the source of free-living Symbiodinium in the environment. In addition, the capacity of host and symbiont to form novel combinations is unknown. To explore patterns of initial association between host and symbiont, larvae of two species of Ac-ropora were exposed to sediment collected from three locations on the Great Barrier Reef. A high proportion of larvae established symbiosis shortly after contact with sediments, and Acropora larvae were promiscuous, taking up multiple types of Symbiodinium. The Symbiodinium types acquired from the sediments reflected the symbiont assemblage within a wide range of cnidarian hosts at each of the three sites, suggesting potential regional differences in the free-living Symbiodinium assemblage. Coral larvae clearly have the capacity to take up Symbiodinium prior to settlement, and sediment is a likely source. Promiscuous larvae allow species to associate with Symbiodinium appropriate for potentially novel environments that may be experienced following dispersal.
a b s t r a c t This paper gives an overview of the value of ecosystem services of 10 main biomes expressed in monetary units. In total, over 320 publications were screened covering over 300 case study locations. Approximately 1350 value estimates were coded and stored in a searchable Ecosystem Service Value Database (ESVD). A selection of 665 value estimates was used for the analysis. Acknowledging the uncertainties and contextual nature of any valuation, the analysis shows that the total value of ecosystem services is considerable and ranges between 490 int/year for the potential services of an 'average' hectare of coral reefs. More importantly, our results show that most of this value is outside the market and best considered as non-tradable public benefits. The continued over-exploitation of ecosystems thus comes at the expense of the livelihood of the poor and future generations. Given that many of the positive externalities of ecosystems are lost or strongly reduced after land use conversion better accounting for the public goods and services provided by ecosystems is crucial to improve decision making and institutions for biodiversity conservation and sustainable ecosystem management.
The late Leonard (Len) Muscatine (1932–2007) played a key role in the development of the understanding of algal-invertebrate
symbioses. For over 40years (1958–2005), Professor Muscatine was an inspirational mentor and leader in this field, guiding
both the ideas and lives of generations of scientists, many of whom are still active in this research area. His scientific
contributions were instrumental in crafting the understanding of a fundamentally important part of our world; that of endosymbiosis,
where two or more independent organisms live together in a cellular harmony that belies a complex set of molecular and evolutionary
interactions. Muscatine’s research career was defined by investigations aimed at unraveling these interactions, particularly
the specificity, metabolism, regulation, and disintegration of algal-invertebrate symbiosis. His gentle interrogation of his
students and colleagues as to “What is the question?” led more than often to the focused research that yielded the insightful
answers that still resonate today as the most current in the field.
The upside-down jellyfish Cassiopea is a globally distributed, semi-sessile, planktonically dispersed scyphomedusa. Cassiopea occurs in shallow, tropical inshore marine waters on sandy mudflats and is generally associated with mangrove-dominated habitats. Controversy over the taxonomy of upside-down jellyfishes precedes their introduction to the Hawaiian Islands during the Second World War, and persists today. Here we address the global phylogeography and molecular systematics of the three currently recognized species: Cassiopea andromeda, C. frondosa, and C. xamachana. Mitochondrial cytochrome c oxidase I (COI) sequences from Australia, Bermuda, Fiji, the Florida Keys, the Hawaiian Islands, Indonesia, Palau, Panama, Papua New Guinea, and the Red Sea were analyzed. Highly divergent COI haplotypes within the putative species C. andromeda (23.4% Kimura 2-parameter molecular divergence), and shared haplotypes among populations of two separate putative species, C. andromeda and C. xamachana from different ocean basins, suggest multiple anthropogenic introductions and systematic confusion. Two deeply divergent Oahu haplotypes (20.3%) from morphologically similar, geographically separate invasive populations indicate long-term (14–40million years ago) reproductive isolation of phylogenetically distinct source populations and cryptic species. Data support at least two independent introductions to the Hawaiian Islands, one from the Indo-Pacific, another from the western Atlantic/Red Sea. Molecular phylogenetic results support six species: (1) C. frondosa, western Atlantic (2) C. andromeda, Red Sea/western Atlantic/Hawaiian Islands (3) C. ornata, Indonesia/Palau/Fiji (4) Cassiopea sp. 1, eastern Australia (5) Cassiopea sp. 2, Papua New Guinea and (6) Cassiopea sp. 3, Papua New Guinea/Hawaiian Islands.
The role of symbiont variation in the photobiology of reef corals was addressed by investigating the links among symbiont
genetic diversity, function and ecological distribution in a single host species, Madracis pharensis. Symbiont distribution was studied for two depths (10 and 25m), two different light habitats (exposed and shaded) and three
host colour morphs (brown, purple and green). Two Symbiodinium genotypes were present, as defined by nuclear internal transcribed spacer 2 ribosomal DNA (ITS2-rDNA) variation. Symbiont
distribution was depth- and colour morph-dependent. Type B15 occurred predominantly on the deeper reef and in green and purple
colonies, while type B7 was present in shallow environments and brown colonies. Different light microhabitats at fixed depths
had no effect on symbiont presence. This ecological distribution suggests that symbiont presence is potentially driven by
light spectral niches. A reciprocal depth transplantation experiment indicated steady symbiont populations under environment
change. Functional parameters such as pigment composition, chlorophyll a fluorescence and cell densities were measured for 25m and included in multivariate analyses. Most functional variation was
explained by two photobiological assemblages that relate to either symbiont identity or light microhabitat, suggesting adaptation
and acclimation, respectively. Type B15 occurs with lower cell densities and larger sizes, higher cellular pigment concentrations
and higher peridinin to chlorophyll a ratio than type B7. Type B7 relates to a larger xanthophyll-pool size. These unambiguous differences between symbionts can
explain their distributional patterns, with type B15 being potentially more adapted to darker or deeper environments than
B7. Symbiont cell size may play a central role in the adaptation of coral holobionts to the deeper reef. The existence of
functional differences between B-types shows that the clade classification does not necessarily correspond to functional identity.
This study supports the use of ITS2 as an ecological and functionally meaningful marker in Symbiodinium.
Three common species of Hawaiian reef corals, Pocillopora damicornis (L.), Montipora verrucosa (Lamarck) and Fungia scutaria Lamarck, were grown in a temperature-regulated, continuous-flow sea water system. The skeletal growth optimum occurred near 26C, coinciding with the natural summer ambient temperature in Hawaii, and was lowest at 21 to 22C, representing Hawaiian winter ambient. Levels of approximately 32C produced mortality within days. Prolonged exposure to temperatures of approximately 30C eventually caused loss of photosynthetic pigment, increased mortality, and reduced calcification. Corals lived only 1 to 2 weeks at 18C. The corals showed greater initial resistance at the lower lethal limit, but ultimately low temperature was more deleterious than high temperature. Results suggest that a decrease in the natural water temperature of Hawaiian reefs would be more harmful to corals than a temperature increase of the same magnitude.
Scyphistomae of Cassiopea andromeda Forskl, 1775 containing symbiontic zooxanthellae did not develop medusae at a constant temperature of 20C, but monodisc strobilation was initiated after transfer of the polyps to 24C. After release of the ephyrae and regeneration of the hypostome and tentacular region, the recovered polyps either produced vegetative buds or entered a new strobilation phase. Formation of motile, planula-like buds was not found to be indicative of unfavourable environmental conditions. Intensity of budding was positively correlated with available food and with increase of temperature. Budding was negatively correlated with the number of polyps maintained per dish and with the conditioning of the sea water. Under optimal feeding and temperature conditions, polyps could simultaneously produce chains of buds at 2 to 4 budding regions. Settlement and development of buds into scyphistomae was suppressed in pasteurized sea water and in pasteurized sea water containing antibiotics, but polyps developed from buds in the presence of algal material taken from the aquarium, debris or egg shells of Artemia salina, or on glass slides which had been incubated in used A. salina culture medium. Several species of marine bacteria were detected after staining these slides. One, a Gramnegative coccoid rod, which was identified as a nonpathogenic Vibrio species, was isolated, cultivated as a pure strain, and was proved to induce the development of C. andromeda buds into polyps. Millipore filter-plates coated with Vibrio sp. cells grown in suspension culture were ineffectual, but diluted filtrate initiated polyp morphogenesis. The inducing factor is obviously not a constituent of the bacterial cell surface, but is a product of growing Vibrio sp. cells released into the medium. This product was found to be relatively heat-stable and dialyzable. As to the basic mechanism involved in the induction of polyp formation, it is suggested that the inducing factor (s) acts bimodally by inducing pedal disc development and by eliminating a head inhibitor originating from the basal end of the bud. The life history, and various aspects of medusa-formation and of vegetative reproduction in scyphozoans are reviewed and discussed with particular reference to rhizostome species. Special attention has been paid to some reports of larval metamorphosis controlled by marine bacteria.
We have investigated whether interactions between cell-surface macromolecules play a role in cellular recognition leading to specificity in the establishment of intracellular symbiosis between dinoflagellates and the polyp (scyphistoma) stage of the jellyfish Cassiopeia xamachana. All strains of the symbiotic dinoflagellate Symbiodinium microadriaticum were phagocytosed by the endodermal cells of the scyphistomae when presented to them as cells freshly isolated from their respective hosts. The rates of phagocytosis of such cells were high, and were directly correlated with the presence of a membrane, thought to be the host cell vacuolar membrane that surrounds the freshly isolated algae. Cultured algae lack this membrane. All cultured algae, even those that proliferate in host tissues, were phagocytosed at very low or undetectable rates. Freshly isolated algae treated with reagents that removed the host membrane were phagocytosed at low rates. The endodermal cells of the scyphistomae of the non-symbiotic medusa Aurelia aurita also phagocytosed freshly isolated algae, but did not phagocytose cultured algae. Phagocytosis of algae and carmine particles was found to be a competitive process in scyphistomae of C. xamachana. No correlation was observed between the surface electrical charge on algae and their phagocytosis by host endodermal cells. Neither was there any correlation between phagocytosis and persistence. We conclude that the specificity in symbioses between marine invertebrates and dinoflagellates appears to be regulated by processes that occur after potential algal symbionts are phagocytosed.
Dinoflagellates in the genus Symbiodinium are best known as endosymbionts of corals and other invertebrate as well as protist hosts, but also exist free-living in coastal environments. Despite their importance in marine ecosystems, less than 10 loci have been used to explore phylogenetic relationships in this group, and only the multi-copy nuclear ribosomal Internal Transcribed Spacer (ITS) regions 1 and 2 have been used to characterize fine-scale genetic diversity within the nine clades (A-I) that comprise the genus. Here, we describe a three-step molecular approach focused on 1) identifying new candidate genes for phylogenetic analysis of Symbiodinium spp., 2) characterizing the phylogenetic relationship of these candidate genes from DNA samples spanning eight Symbiodinium clades (A-H), and 3) conducting in-depth phylogenetic analyses of candidate genes displaying genetic divergences equal or higher than those within the ITS-2 of Symbiodinium clade C. To this end, we used bioinformatics tools and reciprocal comparisons to identify homologous genes from 55,551 cDNA sequences representing two Symbiodinium and six additional dinoflagellate EST libraries. Of the 84 candidate genes identified, 7 Symbiodinium genes (elf2, coI, coIII, cob, calmodulin, rad24, and actin) were characterized by sequencing 23 DNA samples spanning eight Symbiodinium clades (A-H). Four genes displaying higher rates of genetic divergences than ITS-2 within clade C were selected for in-depth phylogenetic analyses, which revealed that calmodulin has limited taxonomic utility but that coI, rad24, and actin behave predictably with respect to Symbiodinium lineage C and are potential candidates as new markers for this group. The approach for targeting candidate genes described here can serve as a model for future studies aimed at identifying and testing new phylogenetically informative genes for taxa where transcriptomic and genomics data are available.
Marine ecosystems are centrally important to the biology of the planet, yet a comprehensive understanding of how anthropogenic
climate change is affecting them has been poorly developed. Recent studies indicate that rapidly rising greenhouse gas concentrations
are driving ocean systems toward conditions not seen for millions of years, with an associated risk of fundamental and irreversible
ecological transformation. The impacts of anthropogenic climate change so far include decreased ocean productivity, altered
food web dynamics, reduced abundance of habitat-forming species, shifting species distributions, and a greater incidence of
disease. Although there is considerable uncertainty about the spatial and temporal details, climate change is clearly and
fundamentally altering ocean ecosystems. Further change will continue to create enormous challenges and costs for societies
worldwide, particularly those in developing countries.
One of the principle ways in which reef building corals are likely to cope with a warmer climate is by changing to more thermally tolerant endosymbiotic algae (zooxanthellae) genotypes. It is highly likely that hosting a more heat-tolerant algal genotype will be accompanied by tradeoffs in the physiology of the coral. To better understand one of these tradeoffs, growth was investigated in the Indo-Pacific reef-building coral Acropora millepora in both the laboratory and the field. In the Keppel Islands in the southern Great Barrier Reef this species naturally harbors nrDNA ITS1 thermally sensitive type C2 or thermally tolerant type D zooxanthellae of the genus Symbiodinium and can change dominant type following bleaching. We show that under controlled conditions, corals with type D symbionts grow 29% slower than those with type C2 symbionts. In the field, type D colonies grew 38% slower than C2 colonies. These results demonstrate the magnitude of trade-offs likely to be experienced by this species as they acclimatize to warmer conditions by changing to more thermally tolerant type D zooxanthellae. Irrespective of symbiont genotype, corals were affected to an even greater degree by the stress of a bleaching event which reduced growth by more than 50% for up to 18 months compared to pre-bleaching rates. The processes of symbiont change and acute thermal stress are likely to act in concert on coral growth as reefs acclimatize to more stressful warmer conditions, further compromising their regeneration capacity following climate change.
Dinoflagellates in the genus Symbiodinium are crucial components of coral reef ecosystems in their roles as endosymbionts of corals and other marine invertebrates. The genus Symbiodinium encompasses eight lineages (clades A-H), and multiple sub-clade types. Symbiodinium in clades A, B, C, and D are most commonly associated with metazoan hosts while clades C, D, F, G, and H with large soritid foraminifera. Recent studies have described a diversity of new Symbiodinium types within each clades, but no new clades have been reported since 2001. Here, we describe a new clade of Symbiodinium isolated from soritid foraminifera from Hawai'i.
The modern synthesis was a seminal period in the biological sciences, establishing many of the core principles of evolutionary biology that we know today. Significant catalysts were the contributions of R.A. Fisher, J.B.S. Haldane and Sewall Wright (and others) developing the theoretical underpinning of population genetics, thus demonstrating adaptive evolution resulted from the interplay of forces such as natural selection and mutation within groups of individuals occupying the same space and time (i.e. a population). Given its importance, it is surprising that detailed population genetic data remain lacking for numerous organisms vital to many ecosystems. For example, the coral reef ecosystem is well recognized for its high biodiversity and productivity, numerous ecological services and significant economic and societal values (Moberg & Folke 1999; Cinner 2014). Many coral reef invertebrates form symbiotic relationships with single-celled dinoflagellates within the genus Symbiodinium Freudenthal (Taylor 1974), with hosts providing these (typically) intracellular symbionts with by-products of metabolism and in turn receiving photosynthetically fixed carbon capable of meeting hosts’ respiratory demands (Falkowski et al. 1984; Muscatine et al. 1984). Unfortunately, the health and integrity of the coral reef ecosystem has been significantly and negatively impacted by onslaughts like anthropogenic eutrophication and disease in addition to global climate change, with increased incidences of ‘bleaching’ events (characterized as the loss of photosynthetic pigments from the algal cell or massive reduction of Symbiodinium density from hosts’ tissue) and host mortality leading to staggering declines in geographic coverage (Bruno & Selig 2007) that have raised questions on the viability of this ecosystem as we know it (Bellwood et al. 2004; Parmesan 2006). One avenue towards anticipating the future of the coral reef ecosystem is by developing a broader and deeper understanding of the current genotypic diversity encompassed within and between populations of their keystone species, the scleractinian corals and dinoflagellate symbionts, as they potentially possess functional variation (either singularly or in combination) that may come under selection due to the ongoing and rapid environmental changes they are experiencing. However, such studies, especially for members of the genus Symbiodinium, are sparse. In this issue, Baums et al. (2014) provide a significant contribution by documenting the range-wide population genetics of Symbiodinium ‘fitti’ (Fig. 1) in the context of complementary data from its host, the endangered Caribbean elkhorn coral Acropora palmata (Fig. 1). Notable results of this study include a single S. ‘fitti’ genotype typically dominates an individual A. palmata colony both spatially and temporally, gene flow among coral host populations is a magnitude higher to that of its symbiont populations, and the partners possess disparate patterns of genetic differentiation across the Greater Caribbean. The implications of such findings are discussed herein.
The mutualistic symbioses between reef-building corals and micro-algae form the basis of coral reef ecosystems, yet recent environmental changes threaten their survival. Diversity in host-symbiont pairings on the sub-species level could be an unrecognized source of functional variation in response to stress. The Caribbean elkhorn coral, Acropora palmata, associates predominantly with one symbiont species (Symbiodinium 'fitti'), facilitating investigations of individual-level (genotype) interactions. Individual genotypes of both host and symbiont were resolved across the entire species' range. Most colonies of a particular animal genotype were dominated by one symbiont genotype (or strain) that may persist in the host for decades or more. While Symbiodinium are primarily clonal, the occurrence of recombinant genotypes indicates sexual recombination is the source of this genetic variation, and some evidence suggests this happens within the host. When these data are examined at spatial scales spanning the entire distribution of A. palmata, gene flow among animal populations was an order of magnitude greater than among populations of the symbiont. This suggests that independent micro-evolutionary processes created dissimilar population genetic structures between host and symbiont. The lower effective dispersal exhibited by the dinoflagellate raises questions regarding the extent to which populations of host and symbiont can co-evolve during times of rapid and substantial climate change. However, these findings also support a growing body of evidence, suggesting that genotype-by-genotype interactions may provide significant physiological variation, influencing the adaptive potential of symbiotic reef corals to severe selection.
The upside-down jellyfish Cassiopea, like many cnidarians, form obligate symbioses with dinoflagellates belonging to the genus Symbiodinium (commonly known as zooxanthellae). In adult Cassiopea, the symbiosis is specific, with a given Cassiopea species hosting a particular symbiont phylotype throughout broad distributions. However multiple phylotypes of Symbiodinium can infect the scyphistoma (polyp) stage of development, making Cassiopea spp. an ideal model to study the effects of symbiont phylotype on host development and proliferation. To assess the flexibility of symbiont acquisition and to understand how symbiont identity affects the early stages of Cassiopea development, symbiont uptake and host developmental traits were monitored in two species of Cassiopea that were exposed to multiple symbiont phylotype in laboratory and field experiments. Scyphistomae of Cassiopea ornata and Cassiopeaxamachana both demonstrated flexibility in their symbiosis at the scyphistoma stage during which they acquired a range of laboratory cultured Symbiodinium. The presence of symbionts in C. ornata increased planuloid production relative to uninfected controls, and the rate at which symbionts accumulated in the polyp tissues varied with symbiont phylotype. Laboratory infected C. xamachana polyps continued to take up novel/additional symbiont types when transferred to the field; however, novel uptake occurred significantly less frequently in polyps that harbored homologous (ITS type-A1) symbionts prior to field placement. Similarly, ephyrae of C. ornata were able to acquire additional symbiont types even when already infected with Symbiodinium ITS type C1. Our findings demonstrate that the symbiosis is flexible within the early ontogeny of Cassiopea, but that associating with the “right” symbiont may provide a developmental advantage for that host.
Adaptations resulting from the possession of endosymbiotic algae enable reef corals to flourish in nutrient-poor tropical waters. The major adaptations are (a) a polytrophic feeding capacity; (b) conservation of nutrients, such as nitrogen, by retention and recycling within a coral head; and (c) acceleration of calcification in the light. The functions of algae and animals thus superimposed result in an association which can exploit the environment better than either associant can alone.
The internal transcribed spacer (ITS) regions from 47 Symbiodinium (Freudenthal) isolates cultured from 34 different host species and two populations sampled from nature were sequenced and compared. Of these, 17 distinct ITS types were identified. The described species Symbiodinium goreaui , S. kawagutii , S. pilosum (Trench and Blank), S. microadriaticum (Freudenthal), and S. ( � Gymnodinium ) linucheae (Trench and Thinh) had ITS sequences distinct from each other. Four of these species share identical ITS sequences with un- characterized isolates. Sequence differences among other isolates indicate that at least seven other cul- tured types await formal species descriptions, whereas numerous others most likely exist in nature. The Sym- biodinium phylogeny is positively correlated with cell size, mycosporine-like amino acid production (UV pro- tection), and host infectivity, whereas the production of water-soluble peridinin-chl a- protein homodimer and monomer apoproteins and isoenzyme similarity do not correlate. There is evidence, based on the lack of phylogenetic congruency with allelic variability, that sexual recombination occurs at some frequency among Symbiodinium populations. Symbiodinium isolates from the Caribbean possess identical ITS sequences to iso- lates originating from the Red Sea or the western Pa- cific. These findings indicate that some Symbiodinium species may have global biogeographic distributions.
Planula larvae of the tropical jellyfish Cassiopea xamachana Bigelow settle and metamorphose on submerged, degrading leaves of the Red Mangrove Rhizophora mangle Linne. Other substrata from the habitat were not settled by the larvae in statistically significant numbers. Planulae preferred the shady side of the leaves, as found in situ, for settlement. Polyps already on the leaves had no influence on settlement behavior of new larvae. Antibiotic treatment of deteriorating mangrove leaves resulted in a significant decrease of the inductive capacity. Boiling of the leaves significantly reduced the number of settled and metamorphosed larvae implying denaturation of the natural inducer. Exposure of leaf fragments in dialysis tubing revealed that the natural cue is water-soluble and smaller than 12 kD. The results of this study indicate that marine bacteria are involved in the production of at least one peptidic inducer originating from the decomposing mangrove leaves.
Colonies of the coral Stylophora pisti11ata growing at high light can obtain all the reduced carbon needed for animal respiration from photosynthesis by symbiotic zooxanthellae.
In contrast, colonies in shaded reef areas must acquire 60% of their reduced carbon heterotrophically. More than 90% of the
carbon fixed by zooxanthellae is translocated to the animal host in both light regimes, but very little is assimilated, apparently
because the translocated products are deficient in nitrogen. Thus, the coral's overall growth efficiency is similar to that
of aquatic herbivores that forage actively.
Members of many invertebrate groups live symbiotically with unicellular algae, but the symbiosis between corals amid dinoflagellate algae (zooxanthelhae) is espe cially interesting because it occurs in all species of tropical reef-buildimig corals ( see reviews by Droop, 1963 ; Yonge, 1963 ; McLaughlin and Zahl, 1966) . Moreover, a significant effect of the algae om-m time physiology of corals has been clearly demon strated and quantified : Corals with symbiotic algae calcify n-many timies faster iii light than in darkness, while corals which have lost their zooxanthelhae calcify at rates which are slower and unaffected by light (Kawaguti and Sakumoto, 1948; Goreau, 1959 ; Goreau and Goreau, 1959) . In the light, photosynthesis by zoo xanthellae must soniehow lead to higher rates of calcification by corals. Three mechanism-mishave been proposed to explain how zooxamithehlae imifluemice coral calcification : ( 1) removal of carbon dioxide in photosymithiesis directly favors chemical equilibria leading to the precipitation of calcium-micarbonate (Goreau, 1959) ; (2) algal removal of phosphates, which n-mayact as crystal poisomis, enhances crystallization of calcium carbonate (Simkiss, 1964a, 1964b) ; and (3) orgamiic products of photosynthesis, either specific mi-materialsrequired for skeletogenesis, or nutrients or general energy sources supplied to the coral, ierm-m-mit faster calcifica tion (Goreau, 1959 ; Wainwright, 1963) . So far, there has been i-moexperimental evidence which conclusively supports or eliminates one hypothesis or another. One observation appears to be inconsistent with current ideas about the inti nate relationship between algal photosynthesis and coral calcification. In tFmestag horn coral, Acropora cervicornis ( Fig. 1) , as in other bramiching forms, calcification rates are highest in the tips, decreasing progressively towards the base (Goreau and Goreau, 1959) . However, very few symbiotic algae are found iii the tips, their numbers increasing towards the base. Where abumidanit, they give the coral a deep brown color, contrasting sharply' with the whiteness of the almost algae-free tips (Figs. 1 and 2). We undertook a study of ti-merapidly calcifying tips in order to clarify the problem of how the algae stimulate coral calcification rates.
▪ Abstract Reef corals (and other marine invertebrates and protists) are hosts to a group of exceptionally diverse dinoflagellate symbionts in the genus Symbiodinium. These symbionts are critical components of coral reef ecosystems whose loss during stress-related “bleaching” events can lead to mass mortality of coral hosts and associated collapse of reef ecosystems. Molecular studies have shown these partnerships to be more flexible than previously thought, with different hosts and symbionts showing varying degrees of specificity in their associations. Further studies are beginning to reveal the systematic, ecological, and biogeographic underpinnings of this flexibility. Unusual symbionts normally found only in larval stages, marginal environments, uncommon host taxa, or at latitudinal extremes may prove critical in understanding the long-term resilience of coral reef ecosystems to environmental perturbation. The persistence of bleaching-resistant symbiont types in affected ecosystems, and the possibilit...
Cassiopea xamachana were bleached by elevated temperature or held in complete darkness. Wet weight was measured over several weeks in bleached and unbleached individuals with or without addition of dissolved organic matter (DOM) and/or particulate organic matter (POM) in a three-factor experiment. Wet weight decreased to a greater extent in temperature-bleached individuals compared to unbleached individuals. Bleaching by darkness produced differences that took longer to manifest themselves compared with temperature bleaching suggesting more than just loss of photosynthetic capability results from heat bleaching. No differences were found between jellyfish based on DOM and/or POM treatments. Heat stress combined with loss of zooxanthellae negatively effects C. xamachana over short time spans indicating the potential for this species to be impacted by natural bleaching events. Cassiopea xamachana could also be a useful model for further study of the effects of bleaching and the recovery.
The use of several independent biochemical, physiological, morphological, and behavioral assays has resulted in the reassessment of the taxonomy of the gymnodinioid symbionts of marine invertebrates which belong to the genus Symbiodinuim Freudenthal (Dinophyceae). The formal description of the type species S. microadriaticum Freudenthal is augmented, and three new species are introduced; S. goreauii, symbiotic with the Caribbean sea anemone Ragactis lucida; S. kawagutii, harbored by the Hawaiian stony coral Montipora verrucosa; and S. pilosum, inhabiting the Caribbean zoanthid Zoanthus sociatus.
SYNOPSIS. The life cycle of the zooxanthella of Cassiopeia sp., as determined by in vitro studies, includes a dominant vegetative autotrophic stage, a reproductive cyst producing autospores, aplanospores, or motile gymnodinioid zoospores, or possible gametes. The predominance of these stages is partially determined by environmental factors, e.g., photoperiodicity. As none of the existing genera of free-living or parasitic algae are wholly applicable to this organism, a new genus, Symbiodinium, is proposed. The type species, S. microadriaticum, is described.
In a recent communication by Stat and Gates (Biol Invasions 10: 579–583, 2008), discovery of a symbiotic combination involving
the coral Acropora cytherea and the dinoflagellate endosymbiont, Symbiodinium
A1 (Symbiodinium microadriaticum, Freudenthal sensu stricto) in the Northwest Hawaiian Islands was interpreted to be the result of a ‘recent’ introduction. While introductions of symbiotic
dinoflagellates have occurred and are occurring, the authors’ conclusion was made without sufficient information about the
geographic range and host specificity exhibited by A1. The only direct genetic analysis of symbionts from the putative host vector, a jellyfish in the genus Cassiopeia sp., from Kaneohe Bay on the Island of Oahu, found that it contained a different symbiont species, A3. Furthermore, Stat and Gates (Biol Invasions 10: 579–583, 2008) did not consider the importance of host-symbiont specificity
in preventing the establishment of a foreign symbiont species. In comparison to A. cytherea, A. longicyathus on the southern most Great Barrier Reef also hosts Symbiodinium
A1 and a closely related endemic, A1a. Instead of assuming that A. cytherea has an unnatural association, a practical explanation is that long-term ecological and evolutionary processes influenced
by local environments underlie the unusual, but not unprecedented finding of a Pacific acroporid associating with Clade A
Symbiodinium spp.
Endosymbiotic dinoflagellates belonging to the genus Symbiodinium associate with a diverse range of marine invertebrate hosts and also exist free-living in the ocean. The genus is divided
into eight lineages (clades A–H), which contain multiple subclade types that show geographic and host specificity. It is commonly
known that free-living dinoflagellates can and have been introduced to new geographic locations, primarily through shipping
ballast water. In this study we sequenced the ITS2 region of Symbiodinium found in symbiosis with the coral Acropora cytherea in the Northwestern Hawaiian Islands Marine National Monument and from shipping ballast water. Identification of an unusual
symbiont in Acropora cytherea and an analysis of the distribution of this symbiont suggests an introduction to Hawaii vectored by the scyphozoan host,
Cassiopea sp. Symbiodinium were also detected in shipping ballast water. This work confirms that marine invertebrate endosymbionts can be introduced
to new geographic locations vectored by animal hosts or the ballast water of ships.
The expulsion of zooxanthellae by octocorals (Xenia macrospiculata and Heteroxenia fuscescens), the scleractinian coral Stylophora pistillata, and the hydrocoral Millepora dichotoma, was measured in the field. The numbers expelled did not exceed 0.1% of the total standing stock of symbiotic algae per day, the rate of expulsion was less than 4% of the rate at which cells are added to symbiotic populations, and the carbon lost represented 0.01% of the total carbon fixed on a daily basis. Expulsion of zooxanthellae is therefore not a significant sink for fixed carbon in these symbiotic associations. In contrast to field populations, expulsion by X. macrospiculata increased 5-fold or more in the laboratory, suggesting that laboratory conditions may introduce stress.
We report an extraordinary depth range for Leptoseris fragilis (Milne Edwards and Haime), a reef building coral of the Red Sea living in cytosymbiosis with zooxanthellae. The coral harbours an as yet unknown pigment system. We suggest that the heterotrophic host — the coral — provides its photoautotrophic symbionts with additional light. The supplementary light is provided by host pigments which transform light of short wavelengths into suitable wavelengths for photosynthesis, thus amplifying and increasing the transfer of photoassimilates from the zooxanthellae to the host.
Scyphopolyps and scyphomedusae of Cassiopea andromeda Forskl (Cnidaria, Scyphozoa) containing dinoflagellate endosymbionts (zooxanthellae) were investigated for rates and pathways of carbon fixation. Photosynthesis by the algae, accounting for 80 and 15 mol C h-1 on a dry weight basis in medusae and polyps, respectively, by far exceeds dark incorporation of inorganic carbon by the intact association. Photosynthetic carbon fixation is operated via C3 pathway of carbon reduction. DCMU-treatment (110-6 M and 110-5 M) completely inhibits light-dependent carbon assimilation. Major photosynthates presumably involved in a metabolite flow from algal symbionts to animal tissue are glycerol and glucose. A total of 5–10% net algal photosynthate appears to be seleased in vivo to the host. This is probably less than the energy supply ultimately required for the nutrition of the polyps and medusae. The presence of zooxanthellae proved to be indispensable for strobilation in the scyphopolyps. However, photosynthesis by algal symbionts as well as photosynthate release is obviously not essential for the initiation of ephyrae as is shown by DCMU-treatment, culture in continous darkness, and aposymbiotic controls. It is therefore concluded that strobilation is supported, but not triggered by algal photosynthetic activity. The induction of strobilation thus seems to depend on a more complex system of regulation.
Morphological variation in qualitative and quantitative features is compared among species of Aurelia defined a priori using molecular criteria. Macro-morphological features were more numerous than previously implied (28 cf. 17), most were variable (26 of 28), and all species were morphologically distinguishable using univariate, multivariate and phylogenetic statistics. However, due to discrepant morphological descriptions, Aurelia spp. 3, 4, and 6 could not be assigned reliably to any previously described species, and there are still insufficient macro-morphological characters and variation to reconstruct a statistically robust phylogeny for even the 12 known species of Aurelia. Yet it is shown that Aurelia aurita is most likely endemic to the boreal Atlantic Ocean and northern European seas, Aurelia labiata is neither as morphologically diverse nor widespread as recently described, and the circumglobal Aurelia sp. 1 is probably introduced across much of its range.
The jellyfish Cassiopea xamachana often contains a blue pigment diffused within the acellular portion of its masoglea. In the bell, both the pigment and endosymbiotic zooxanthellae are concentrated immediately beneath the ex-and subumbrellar epithelia. Chromatographic and polyacrylamide gel electrophoretic techniques demonstrate that the pigment is a highly polymeric glycoprotein (mol. wt>106 daltons) comprised of two subunits with molecular weights of 34 500 and 30 300 daltons and characterized by multiple charged species. The blue native protein exhibits light absorption maxima at 620, 587, 555 and 415 nm, while SDS denatured protein is pink with a single absorption maximum at 507 nm. No prosthetic chromophore or heavy metal component was detected. The pigment is proposed to act as a light attenuator protecting the jellyfish from injurious solar irradiation while allowing photosynthetically active wavelengths to reach the zooxanthellae.
The blue mesogleal pigment of the symbiotic jellyfish, Cassiopea xamachana Bigelow, 1882, is composed of two subunits, a larger glycosylated (35kDa) moiety and a non-glycosylated (30kDa) variant in lower concentration. In solution, the subunits assemble in large complexes of at least 106kDa. The pigment, known as Cassio Blue, appears to mitigate excessive solar radiation while allowing the passage of the wavelengths optimal for photosynthesis by the numerous algal symbionts in the mesoglea of the jellyfish. The pigment is an abundant protein comprising about 6% of all animal protein in the whole jellyfish and about 33% of all animal protein in the oral appendages. The protein also contains a diverse array of metals, notably Ag, Ca, Cu, Fe, Mg, and Zn, with traces of others. Metal stoichiometry varies among isolates averaging about 1mol of all metals, taken together, for each mole of the pigment. Given the broad array of metals present, the pigment may also serve another purpose, for example, as a metal reservoir or trap. Few other proteins are associated with such a spectrum of metals. In addition, the amino acid sequences of the pigment tryptic peptides have no reasonable matches in any of the sequence databases. Our findings, taken as a whole, suggest that the Cassio pigment is indeed unusual and is likely a representative of a novel category of proteins, the original member of which is rpulFKz1, a chromoprotein endowed with Frizzled and Kringle domains.
The rate of loss of zooxanthellae from intact Pocillopora damicornis (Linnaeus) was determined for colonies growing in laboratory tanks supplied with either ambient seawater or seawater enriched with dissolved inorganic N. Algal release peaked during midday in both treatments. Corals in N-enriched water released 40% more algae · U−1 surface area · day−1 than did control corals. However, algal densities in the N-enriched corals were three times higher than in controls, so specific release rate was lower for N-enriched corals. Lipid content of the N-enriched corals was also lower than in the controls. These results suggest that N enrichment results in: greater algal standing stock and a reduced rate of transfer of photosynthate to the host. N enrichment more than doubled algal densities in this coral indicating that zooxanthellae in situ may be nutrient limited and that algal densities are, to some extent, a function of nutrient levels in the external environment and not entirely regulated by the host.
Marine invertebrates representing at least five phyla are symbiotic with dinoflagellates from the genus Symbiodinium. This group of single-celled protists was once considered to be a single pandemic species, Symbiodinium microadriaticum. Molecular investigations over the past 25 years have revealed, however, that Symbiodinium is a diverse group of organisms with at least eight (A–H) divergent clades that in turn contain multiple molecular subclade types. The diversity within this genus may subsequently determine the response of corals to normal and stressful conditions, leading to the proposal that the symbiosis may impart unusually rapid adaptation to environmental change by the metazoan host. These questions have added importance due to the critical challenges that corals and the reefs they build face as a consequence of current rapid climate change. This review outlines our current understanding of the diverse genus Symbiodinium and explores the ability of this genus and its symbioses to adapt to rapid environmental change.
The ability to acquire different types of the symbiotic dinoflagellate Symbiodinium (zooxanthellae) from the environment was investigated using aposymbiotic scyphistomae of the jellyfish Cassiopea xamachana. Non-symbiotic scyphistomae were placed on an offshore Florida patch reef and in Florida Bay during 3- and 5-day periods in March, and 5-day exposures in May, August and December of 2003. Scyphistomae were maintained in culture for several months, after which members of clades A, B, C and D Symbiodinium were detected in these hosts by denaturing gradient gel electrophoresis (DGGE) analyses. These findings contrast with naturally collected C. xamachana medusa from Florida Bay where all specimens possessed only Symbiodinium type A1. Furthermore, the polyps did not acquire the symbionts found in nearby cnidarian colonies, suggesting that a diverse pool of symbiont lineages exists in the environment. These results support previous laboratory studies where aposymbiotic hosts were initially non-selective and capable of acquiring many kinds of Symbiodinium. The specificity seen in adult hosts is likely a result of post-infection processes due to competitive exclusion or other mechanisms. A higher percentage of polyps became infected after 5 days of exposure, compared to 3 days, and no infections were observed in laboratory controls held in filtered seawater. Infections were lowest (50% at both sites) in March of 2003, when seawater temperatures were at their annual minima. Infection was 100% in scyphistomae exposed for 5 days during the months of May, August and December of 2003. These findings suggest that this host system, in addition to addressing questions of host-symbiont selectivity, can be employed to monitor and define the abundance and distribution of natural pools of Symbiodinium.
The influence of light intensity on the fatty acid profiles of the scyphozoan jellyfish Cassiopea sp. and its endosymbiotic zooxanthellae was investigated using a manipulative experiment. The aims of the study were to: 1) identify changes related to light intensity in the fatty acid profiles of the host jellyfish and zooxanthellae; 2) determine if jellyfish exposed to low light intensities compensated for reduced rates of photosynthesis by increasing heterotrophic feeding; and 3) determine if concentrations of zooxanthellae and chlorophyll a (chl a) increased in jellyfish exposed to reduced light intensity. Jellyfish were collected from an artificial urban tidal lake in southeast Queensland, Australia. Two were frozen for immediate analysis and 15 were randomly allocated to each of nine mesocosms. Three replicate mesocosms were then randomly allocated to each of three light treatments: 100%, 25%, and 10% PAR. The mesocosms were supplied with unfiltered, continuous flowing seawater and jellyfish fed on natural zooplankton, supplemented with frozen Mysis shrimp. Three jellyfish were sampled, with replacement, from each mesocosm 3, 15, 22, 39 and 69 days after the experiment commenced. Fatty acids as methyl esters in the host tissue (mesoglea) and zooxanthellae were determined separately using gas chromatography and verified by mass spectrometry. The fatty acid profiles of the host jellyfish and zooxanthellae remained unchanged in the 100% PAR treatment throughout the experiment but varied in the lower light treatments. A decrease in light intensity caused a reduction in the concentrations of some polyunsaturated fatty acids such as 18:1ω9 and 18:4ω3 in the zooxanthellae, the latter being abundant in dinoflagellates. Concomitantly, the concentrations of these fatty acids increased in the host tissues, suggesting a possible transfer of zooxanthellate fatty acids to the jellyfish. Jellyfish in the 10% PAR treatment shrank during the experiment and their fatty acid profiles did not reflect any shift towards increased heterotrophy. On days 22 and 69 concentrations of chl a, zooxanthellae and [chl a] zooxanthella− 1 were determined. [chl a] and [chl a] zooxanthella− 1, initially increased in the lower light treatments but decreased by the end of the experiment indicating that jellyfish may adapt to reduced light intensity in the short-term but that long-term exposure to reduced light results in compromised performance.
Reef-building corals occur as a range of colour morphs because of varying types and concentrations of pigments within the host tissues, but little is known about their physiological or ecological significance. Here, we examined whether specific host pigments act as an alternative mechanism for photoacclimation in the coral holobiont. We used the coral Montipora monasteriata (Forskål 1775) as a case study because it occurs in multiple colour morphs (tan, blue, brown, green and red) within varying light-habitat distributions. We demonstrated that two of the non-fluorescent host pigments are responsive to changes in external irradiance, with some host pigments up-regulating in response to elevated irradiance. This appeared to facilitate the retention of antennal chlorophyll by endosymbionts and hence, photosynthetic capacity. Specifically, net P(max) Chl a(-1) correlated strongly with the concentration of an orange-absorbing non-fluorescent pigment (CP-580). This had major implications for the energetics of bleached blue-pigmented (CP-580) colonies that maintained net P(max) cm(-2) by increasing P(max) Chl a(-1). The data suggested that blue morphs can bleach, decreasing their symbiont populations by an order of magnitude without compromising symbiont or coral health.
Endosymbiotic dinoflagellates, or "zooxanthellae," are required for the survival of a diverse community of invertebrates that construct and dominate shallow, tropical coral reef ecosystems. Molecular systematics applied to this once understudied symbiont partner, Symbiodinium spp., divide the group into divergent lineages or subgeneric "clades." Within each clade, numerous closely related "types," or species, exhibit distinctive host taxon, geographic, and/or environmental distributions. This diversity is greatest in clade C, which dominates the Indo-Pacific host fauna and shares dominance in the Atlantic-Caribbean with clade B. Two "living" ancestors in this group, C1 and C3, are common to both the Indo-Pacific and Atlantic-Caribbean. With these exceptions, each ocean possesses a diverse clade C assemblage that appears to have independently evolved (adaptively radiated) through host specialization and allopatric differentiation. This phylogeographic evidence suggests that a worldwide selective sweep of C1/C3, or their progenitor, must have occurred before both oceans separated. The probable timing of this event corresponds with the major climactic changes and low CO(2) levels of the late Miocene and/or early Pliocene. Subsequent bursts of diversification have proceeded in each ocean since this transition. An ecoevolutionary expansion to numerous and taxonomically diverse hosts by a select host-generalist symbiont followed by the onset of rapid diversification suggests a radical process through which coral-algal symbioses respond and persist through the vicissitudes of planetary climate change.
The specific identity of endosymbiotic dinoflagellates (Symbiodinium spp.) from most zooxanthellate corals is unknown. In a survey of symbiotic cnidarians from the southern Great Barrier Reef (GBR), 23 symbiont types were identified from 86 host species representing 40 genera. A majority (>85%) of these symbionts belong to a single phylogenetic clade or subgenus (C) composed of closely related (as assessed by sequence data from the internal transcribed spacer region and the ribosomal large subunit gene), yet ecologically and physiologically distinct, types. A few prevalent symbiont types, or generalists, dominate the coral community of the southern GBR, whereas many rare and/or specific symbionts, or specialists, are found uniquely within certain host taxa. The comparison of symbiont diversity between southern GBR and Caribbean reefs shows an inverse relationship between coral diversity and symbiont diversity, perhaps as a consequence of more-rapid diversification of Caribbean symbionts. Among clade C types, generalists C1 and C3 are common to both Caribbean and southern GBR symbiont assemblages, whereas the rest are regionally endemic. Possibly because of environmental changes in the Caribbean after geographic isolation through the Quaternary period, a high proportion of Caribbean fauna associate with symbiont taxa from two other distantly related Symbiodinium clades (A and B) that rarely occur in Pacific hosts. The resilience of Porites spp. and the resistance of Montipora digitata to thermal stress and bleaching are partially explained by their association with a thermally tolerant symbiont type, whereas the indiscriminant widespread bleaching and death among certain Pacific corals, during El Nino Southern Oscillation events, are influenced by associations with symbionts possessing higher sensitivity to thermal stress.