Review of the diversity, traits, and ecology of zooxanthellate jellyfishes

Abstract

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. 6 Box 3: Glossary We give here some of the technical terms used in this review. For more information on jellyfish anatomy, development and taxonomy, see Arai 1997 and Bouillon et al. 2006.

Cnidarian Pattern Recognition Receptor Repertoires Reflect Both Phylogeny and Life History Traits

“…Three of these life history traits, intracellular algal symbiosis, coloniality, and sedentary lifestyle, we found to have a significant association with total number of PRRs. While intracellular algal symbiosis occurs in both Medusozoa and Anthozoa, there are far more symbiotic anthozoan genera ( 18 , 124 ). The establishment and maintenance of intracellular algal symbionts is a complex process, with many cnidarian species hosting several species of algae, and thus it likely requires immune specificity ( 18 ).…”

High photosynthetic plasticity may reinforce invasiveness of upside-down zooxanthellate jellyfish in Mediterranean coastal waters

“…Symbionts in Cassiopea specimens were identified as belonging to the Cladocopium genus (formerly clade C), the taxon with the highest species richness and the most ecologically and physiologically diversified within the family Symbiodiniaceae, hosted also by sponges, corals and other cnidarians, flatworms and bivalves, as well as by protists (ciliates and foraminiferans) [ 15 ]. In Cassiopea , Cladocopium is often associated to Symbiodinium and Breviolum (reviewed by Djeghri et al [ 23 ]). Incubation at the two different light conditions (irradiance 200 vs 500 μmol photons m -1 s -1 ) did not produce a significant difference in symbiont abundance ( Fig 1 ).…”

“…[ 19 , 20 ], the spotted jellyfish Phyllorhiza punctata [ 21 ], and the golden jellyfish Mastigias papua , where up to 10% of its protein biomass is produced by their endosymbiotic dinoflagellates [ 22 ]. This mutualistic association grants jellyfish a mixotrophic strategy (i.e., based on concurrent heterotrophic and autotrophic energy inputs) [ 23 ]. Mutualism is realized by jellyfish providing a sheltered habitat—rich in nitrogen and phosphorus catabolites—to microalgae that, in turn, release organic carbon products (e.g., sugars) to their host [ 24 , 25 ].…”

“…Mutualism is realized by jellyfish providing a sheltered habitat-rich in nitrogen and phosphorus catabolites-to microalgae that, in turn, release organic carbon products (e.g., sugars) to their host [24,25]. Mixotrophy may be considered as the dominant feeding strategy for symbiotic jellyfish, however the relative importance of autotrophic versus heterotrophic nutrition is variable not only among species, but also within each species' life cycle and depending on seasonality [23]. In most cases, photosynthesis largely covers the respiratory needs, and assimilation of additional inorganic nutrients is required from the surrounding water column [26][27][28].…”

Isotopic and elemental compositions reveal density‐dependent nutrition pathways in a population of mixotrophic jellyfish

“…These marine lakes, especially Ongeim’l Tketau with its jellyfish population, offer an opportunity as model systems for the investigation of density‐dependent dynamics impacting the nutrition of mixotrophic organisms. Zooxanthellate jellyfishes in general, including Mastigias , can show important variability in their nutrition (reviewed in Djeghri et al 2019). The population of medusae in Ongeim’l Tketau can be large (in the order of tens of individuals per m 2 , Hamner et al 1982, Cimino et al 2018) and are a key driver of community dynamics (Wollrab et al 2019).…”