High trophic plasticity in the mixotrophic Mastigias papua-Symbiodiniaceae holobiont: implications for the ecology of zooxanthellate jellyfishes

Abstract

The trophic ecology of mixotrophic, zooxanthellate jellyfishes potentially spans a wide spectrum between autotrophy and heterotrophy. However, their degree of trophic plasticity along this spectrum is not well known. To better characterize their trophic ecology, we sampled the zooxanthellate medusa Mastigias papua in contrasting environments and sizes in Palau (Micronesia). We characterized their trophic ecology using isotopic (bulk δ13C and δ15N), elemental (C:N ratios), and fatty acid compositions. The different trophic indicators were correlated or anti-correlated as expected (Pearson’s correlation coefficient, rP > 0.5 or < -0.5 in 91.1% of cases, p < 0.05), indicating good agreement. The sampled M. papua were ordered in a trophic spectrum between autotrophy and heterotrophy (supported by decreasing δ13C, C:N, proportion of neutral lipid fatty acids (NLFA:TLFA), n-3:n-6 and increasing δ15N, eicosapentaenoic acid to docosahexaenoic acid ratio (EPA:DHA)). This trophic spectrum was mostly driven by sampling location with little influence of medusa size. Moreover, previous observations have shown that in a given location, the trophic ecology of M. papua can change over time. Thus, the positions on the trophic spectrum of the populations sampled here are not fixed, suggesting high trophic plasticity in M. papua. The heterotrophic end of the trophic spectrum was occupied by non-symbiotic M. papua, whereas the literature indicates that the autotrophic end of the spectrum corresponds to dominant autotrophy, where more than 100% of the carbon requirement is obtained by photosynthesis. Such high trophic plasticity has critical implications for the trophic ecology and blooming ability of zooxanthellate jellyfishes.

Understanding Cassiopea andromeda (Scyphozoa) Invasiveness in Different Habitats: A Multiple Biomarker Comparison

“…As C:N ratios demonstrated, jellyfish in the shrimp farm seemed to move from an autotrophic-mixotrophic strategy (C:N 5.36 ± 0.23) to a more heterotrophic one at the end of the rainy season (C:N 3.81 ± 0.05). [15] reported a similar behavior in the symbiotic M. papua, where jellyfish populations showed instead different autotrophy/heterotrophy contributions based on the sampling location, in Palau [15].…”

“…The total fatty acids (FA) of jellyfish from the two habitats were analyzed only in the last sampling time (October) in which both populations were present due to a lack of DW from the July sampling; thus, the methodology and results are reported in the Supplementary Materials. Both stable isotope (δ 15 N and δ 13 C) composition and the carbon/nitrogen (C:N) mass ratio were assessed in three umbrella samples [46] collected at the shrimp farm and the mangrove estuarine ecosystem on each sampling date (n = 18, Table 2). Approximately 1.8-2 mg of DW was introduced in tin capsules to run each sample separately, and analyses were performed using the Elementar IsoPrime 100 isotope ratio-mass spectrometry (IR-MS) instrument (IsoPrime Ltd., Cheadle Hulme, UK) coupled to an N-C-S elemental analyzer (Elementar Vario Pyro Cube EA CNS; Elementar Analysensysteme GmbH, Hanau, Germany).…”

“…Cassiopea andromeda couples typical heterotrophic feeding based on zooplankton, POM (particulate organic matter), DOM (dissolved organic matter) and detritus, with an additional autotrophic energy supply from its endosymbiotic dinoflagellates [50,53,54]. In mixotrophic metazoans, stable isotope analysis and C:N ratios can contribute as nutritional indicators to unravel the predominant trophic strategy, as well as the nutrient exchanges between host and endosymbionts [15,55,56]. In our study, a significant difference was observed between the two environments, with δ 13 C values lower in jellyfish tissues from mangroves (July: Sf −19; M −20; October: Sf −16; M −18).…”

“…It is characterized by a mutualistic association with dinoflagellate microalgae (Symbiodiniaceae), which are able to adapt to different light conditions and provide the jellyfish with carbohydrates and lipids of photosynthetic origin, in return for a sheltered area with a regular supply of inorganic molecules [12][13][14]. The possibility of relying on different energy inputs (i.e., photosynthates from symbionts and heterotrophic input) allows C. andromeda to adapt to different environmental conditions with cascading consequences on primary productivity, nutrient cycling, and local food webs as observed in other symbiotic jellyfish species [15]. The study of animal diet (heterotrophic input) has been widely applied to understand the metazoan trophic interactions in food webs [16][17][18][19][20].…”

“…This may be the case with C. andromeda. A combination of biomarkers (δ 13 C and δ 15 N, fatty acids, and lipid-carbohydrate storage) has been already used to understand the trophic position and the nutritional condition of both Semaeostomeae and Rhizostomeae jellyfish species such as Aurelia aurita, Stomolophus meleagris, and Cyanea nozakii [30]; Chrysaora melanaster [31]; Catostylus mosaicus [27]; Pelagia noctiluca [19,32,33]; and Mastigias papua [15]. It has thus been demonstrated to be a reliable and robust approach, especially in the understanding of jellyfish invasiveness potential under contrasting coastal habitats or environmental conditions.…”