Influence of resource availability on zooxanthellate and nonzooxanthellate scyphozoan polyps: Similar budding and survival responses of Cassiopea sp. and Aurelia sp.

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Diversity of Symbionts

Zooxanthellae associated with jellyfish species belong mostly to the family Symbiodiniaceae (see the recent revision of the family by LaJeunesse et al. (2018)). The most common symbionts found in zooxanthellate scyphozoan jellyfishes in the field appear to belong to the genera Symbiodinium (previously Symbiodinium clade A) and Cladocopium (previously Symbiodinium clade C) although other Symbiodiniaceae can be found (LaJeunesse et al. 2001, Santos et al. 2003, Thornhill et al. 2006, Mellas et al. 2014). Furthermore, laboratory experiments have demonstrated that the associations between the jellyfish Cassiopea spp. and Symbiodiniaceae genera are not specific. 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) (Thornhill et al. 2006, 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 (Thornhill et al. 2006). Thus some flexibility appears to exist in the zooxanthellae-jellyfish association. This is further illustrated by the symbionts found in the hydrozoan Velella velella. Zooxanthellae from Velella velella can indeed belong to Symbiodiniaceae (LaJeunesse et al. 2001) but they can also belong to the genera Brandtodinium and Scrippsiella (or Ensiculifera) from the family Thoracosphaeraceae (Banaszak et al. 1993, Probert et al. 2014).

Biogeography and Habitat

Generally, zooxanthellate jellyfishes are found in tropical and sub-tropical waters between 40° N and 40° S (see e.g. Bieri 1977, Bouillon et al. 1988, Bolton and Graham 2004, Holland et al. 2004, Bayha and Graham 2014, Heins et al. 2015, Straehler-Pohl and Toshino 2015, Boero et al. 2016, Swift et al. 2016). The zooxanthellate coronates and kolpophoran rhizostomes in particular are tropical clades (Dawson and Hamner 2009). However, exceptions can exist as some zooxanthellate jellyfishes may be found in temperate waters either occasionally (e.g. Purcell et al. 2012a) or possibly as resident species (see Brinckmann-Voss and Arai 1998).
At finer geographic scales, zooxanthellate jellyfishes are typically shallow-water species (Dawson and Hamner 2009). They have been reported in a number of coastal habitats including lagoons, estuaries, coral reefs, mangroves or marine lakes (see e.g. García 1990, Kikinger 1992, Fleck and Fitt 1999, Pitt et al. 2004, Swift et al. 2016, Morandini et al. 2017). Such coastal habitats are most likely linked to the fact that most zooxanthellate jellyfishes have a benthic polyp phase, which limits their extension toward the open ocean. However, the medusa phase in some instances has been reported in the open sea (e.g. in Cepheidae – Tokioka et al. 1964, Boero et al. 2016, in Linuche – Larson 1992). Furthermore, hydrozoans of the family Porpitidae realize their whole life-cycle in the open ocean (Bieri 1977), exemplifying that the presence of benthic polyps in the life-cycle, rather than symbiosis with zooxanthellae, more likely restricts jellyfishes to coastal waters.

Acquisition, Location, Transmission and Abundance of Zooxanthellae along the Jellyfish Life-Cycle

The acquisition of zooxanthellae is the first step of the symbiosis. A host may acquire zooxanthellae by two means: (1) vertical transmission, where the symbiont is directly transferred from the parents to the offspring (usually from the mother to the egg), or (2) horizontal transmission, where the symbiont is taken from the environment. While vertical transmission may occur in zooxanthellate hydrozoans (see e.g. Mangan 1909, Bouillon 1984, Lewis 1991), it is likely that most other zooxanthellate jellyfishes acquire their symbionts via horizontal transmission. In Kolpophorae, the symbiont is not provided by parents but acquired from the environment at the polyp stage (e.g. Sugiura 1963, Ludwig 1969, Sugiura 1969, Fitt 1984, Colley and Trench 1985, Kikinger 1992, Astorga et al. 2012, Newkirk et al. 2018). The coronate Linuche unguiculata presents a somewhat intermediate mode of acquisition of the symbiont since fertilized eggs are released in mucus strand replete with maternal zooxanthellae that contaminate the larvae very early in development, generally before the 128 cells stage (Montgomery and Kremer 1995).

Location of zooxanthellae in jellyfishes

In hydromedusae, zooxanthellae are found in endodermal cells (Bouillon et al. 1988, Banaszak et al. 1993, see also Brooks 1903, Brinckmann-Voss and Arai 1998, Fig. 2a). In scyphozoans, zooxanthellae first enter pol ps’ e doder al ells, which then migrate and become mesogleal amaebocytes (Colley and Trench 1985, Fig. 2a and b). In ephyrae, these amaebocytes filled with zooxanthellae stay mostly closely associated with the endoderm (see Kikinger 1992, Silveira and Morandini 1998, Straehler-Pohl and Jarms 2010). This remains the case for later stage medusae in the Coronatae (Linuche unguiculata; Costello and Kremer 1989), and in the Cepheidae (Cotylorhiza tuberculata; Kikinger 1992). In other, non-cepheid, Kolpophorae, the zooxanthellae end up closely associated with the ectoderm (e.g. coronal muscle, subumbrella, exumbrella, oral arms; Blanquet and Riordan 1981, Muscatine et al. 1986, Blanquet and Phelan 1987, Estes et al. 2003, Souza et al. 2007, Fig. 2c). This suggests that the close association of zooxanthellae with the ectoderm could be a synapomorphy of the clade of non-cepheid Kolpophorae. The reason for this evolution is unclear, but perhaps could have adaptive value in allowing better exposure of zooxanthellae to light or nutrients, or providing energy more directly to the host tissues that require it the most.

Abundance and transmission of the zooxanthellae during the jellyfish life-cycle

Zooxanthellae abundance in their hosts is affected by the complex life-cycles of jellyfishes. In the best studied zooxanthellate jellyfishes, the Kolpophorae, the symbionts are taken up at the polyp stage. At this stage, the abundance of zooxanthellae can range from zero (aposymbiotic polyp) to tens of thousands of zooxanthellae per polyp (Newkirk et al. 2018). Polyps form other polyps asexually through a variety of processes (e.g. Schiariti et al. 2014) and in Kolpophorae, the dominant process is by far the production of planuloid buds (Schiariti et al. 2014, Heins et al. 2015). During this process, zooxanthellae are transferred from the parent polyp to the forming bud. Thus polyps formed asexually by zooxanthellate polyps are also zooxanthellate (e.g. Sugiura 1964, Ludwig 1969, Silveira and Morandini 1998, Heins et al. 2015). Then, during strobilation, zooxanthellae multiply in the oral region of the polyp where the ephyra is formed (Ludwig 1969). The ephyrae formed are thus also zooxanthellate (e.g. Sugiura 1964, Ludwig 1969, Sugiura 1969, Kikinger 1992, Silveira and Morandini 1997, 1998, Straehler-Pohl and Jarms 2010). Finally, during the growth of medusae, zooxanthellae densities tend to stay constant or to decrease slightly in most species (densities in the order of 107 cells.g-1 wet mass, see Muscatine et al. 1986, Kremer et al. 1990, Verde and McCloskey 1998). However, some species such as Cephea cephea may lose their zooxanthellae at the medusae stage (Sugiura 1969); this is likely the case of many other Cepheidae too (see Appendix). The ontogenic loss of zooxanthellae suggests that the symbiosis might present trade-offs and might not always be advantageous (see e.g. Lesser et al. 2013). The presence or absence of zooxanthellae during the life-cycle of some zooxanthellate jellyfish have been.

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Nutrition of Zooxanthellate Jellyfishes

Zooxanthellate jellyfishes differ from non-zooxanthellate jellyfishes by the additional energy source they can access through the photosynthesis of their zooxanthellae (either through exchange of metabolites but also through digestion of zooxanthellae, see Davy et al. 2012). In polyps however, only a small part of photosynthates is directed to the host (Hofmann and Kremer 1981). At the medusae stage, by contrast, photosynthesis can constitute an important, if not the major part, of the nutrition of zooxanthellate medusae. Photosynthetic rates are often equal or superior to respiration rates (Drew 1972, Cates 1975, Mergner and Svoboda 1977, Kremer et al. 1990, Kikinger 1992, McCloskey et al. 1994, Verde and McCloskey 1998, Welsh et al. 2009, Jantzen et al. 2010). This indicates that in most cases, respiration requirements in carbon may be fulfilled, and even exceeded, by the photosynthetic activity.
When the holo io t’s photosynthesis rates exceed respiration rates, the host’s metabolites cannot fulfill the photosynthetic demand of zooxanthellae. Thus zooxanthellate jellyfishes must take additional inorganic nutrients (inorganic carbon, nitrogen or phosphorus) from the surrounding water (reviewed in Pitt et al. 2009, see Hofmann and Kremer 1981, Muscatine and Marian 1982, Wilkerson and Kremer 1992, Pitt et al. 2005, Todd et al. 2006, Welsh et al. 2009, Jantzen et al. 2010, Freeman et al. 2016). Uptake rates of various nutrients can be influenced by some environmental factors. For instance, darkness can induce net nitrogen excretion (Cates and McLaughlin 1976, Pitt et al. 2005, Welsh et al. 2009 but see Muscatine and Marian 1982, Wilkerson and Kremer 1992), while light has been found to increase ammonium and inorganic carbon uptake (Jantzen et al. 2010, Freeman et al. 2016). All this indicates that photosynthetically active zooxanthellae play an important role in inorganic nutrient uptake.
Given the nutritional importance of the symbionts, it is not surprising that their hosts present some behavioral and morphological characteristics that help their zooxanthellae (see e.g. Furla et al. 2011 for scleractinian corals). Zooxanthellate jellyfishes, for instance, tend to maximize their light exposure by swimming near the surface (e.g. Hamner et al. 1982, Larson 1992, Haddad and Nogueira Júnior 2006 but see Bieri 1977), but also by performing more complex horizontal and vertical daily migrations (Hamner and Hauri 1981, Hamner et al. 1982, Dawson and Hamner 2003). Similarly, zooxanthellae patches found in Linuche unguiculata tissue contract with a daily rhythm (Costello and Kremer 1989). One consequence of these behaviors is high exposure to potentially damaging UV radiation. It has thus been h pothesized that so e zoo a thellate jell fishes’ pig e ts ight ha e a photoprote ti e role (Blanquet and Phelan 1987, Dawson 2005 but see Lampert et al. 2012) as might small behavioral adjustments of depth (Dawson and Hamner 2003). Other behavioral and morphological characteristics of zooxanthellate medusae have been suggested to help their zooxanthellae to access inorganic nutrients. For instance, zooxanthellae within their hosts are found in high concentration near the coronal muscle, which is an important source of excretion products (Blanquet and Riordan 1981, Muscatine et al. 1986, Blanquet and Phelan 1987). The zooxanthellate jellyfish Mastigias papua performs reverse diel vertical migrations (Hamner et al. 1982, Tomascik and Mah 1994, Dawson and Hamner 2003) which help it to access deep nutrients at night in stratified environments (Hamner et al. 1982, Muscatine and Marian 1982), possibly imprinting a daily rhythm in the cell division of its symbionts (Wilkerson et al. 1983). And finally, the pumping action of Cassiopea facilitates its access to nutrient-rich pore water (Jantzen et al. 2010). Additional access to nitrogen might also be provided by symbiotic nitrogen fixing bacteria (Freeman et al. 2017).

Table of contents :

General introduction / Introduction générale 
1. Jellyfishes in marine ecosystems
2. Role of jellyfish specific life-cycles and body-plans for their population dynamics
3. Heterotrophic nutrition of jellyfishes
4. Nutrition of zooxanthellate jellyfishes, and the structure and objectives of this thesis
Chapter I: Review of the diversity, traits, and ecology of zooxanthellate jellyfishes
1. Introduction
2. Diversity of zooxanthellate jellyfishes
3. Roles of the zooxanthellae in jellyfish symbioses
4. Ecology of zooxanthellate jellyfishes
5. Summary and knowledge gaps
Chapter II: Influence of resource availability on zooxanthellate and nonzooxanthellate scyphozoan polyps: Similar budding and survival responses of Cassiopea sp. and Aurelia sp.
1. Introduction
2. Materials and methods
3. Results
4. Discussion
Chapter III: δ13C, δ15N, and C:N ratios as nutrition indicators of zooxanthellate jellyfishes: insights from an experimental approach
1. Introduction
2. Materials and methods
3. Results
4. Discussion
Chapter IV: Photosy􀅶thesis or predatio􀅶? Nutritio􀅶al plasticity of Palau’s Mastigias papua (Scyphozoa: Rhizostomeae) using stable isotopes and fatty acids
Photosy􀅶thesis or predatio􀅶? Nutritio􀅶al plasticity of Palau’s Mastigias papua (Scyphozoa: Rhizostomeae) using stable isotopes and fatty acids
1. Introduction
2. Materials and methods
3. Results
4. Discussion
General discussion / Discussion générale 
1. Introduction
2. Scientific contributions of this thesis
3. Implications for the ecology of zooxanthellate jellyfishes
4. Knowledge gaps and future directions
5. Conclusions
Appendix 

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