Variation in δ13C and δ15N values suggests a coupling of host and symbiont metabolism in the Symbiodinium-Cassiopea mutualism

: While the ‘upside-down’ jellyfish Cassiopea xamachana feeds heterotrophically, its energy requirements are likely met through its symbiosis with the dinoflagellate symbiont Symbiodinium . To investigate the potential coupling of host and symbiont metabolism within C. xama chana , we assessed whether variation in the isotope values ( δ 13 C and δ 15 N) of photosymbiont-rich oral arm tissue was reflected in bell tissue, which is predominately composed of thick animal mesoglea. Samples were collected from 5 geographically disparate sites, including a site influenced by anthropogenically-derived nutrients. Oral arm δ 13 C values were variable across sites, reflecting varying inputs of marine, terrestrial, and seagrass-derived carbon. Low (<0‰) δ 15 N values of oral arm tissue at the 4 non-impacted sites suggests nitrogen derived from nitrogen fixation, while high (~6‰) δ 15 N values from the impacted site suggests the assimilation of 15 N-enriched sources like sewage. Oral arm δ 13 C and δ 15 N values accounted for ~75 and 25% of the variation in bell δ 13 C and δ 15 N values. The translocation of symbiont-derived carbon and nitrogen to the host was also supported by evidence of trophic enrichment, with bell tissue enriched on average by 1.7 and 3.4‰ compared to oral arm tissue for δ 13 C and δ 15 N, respectively. These data support the contention that microbial symbionts within Cassiopea are critical to productivity and nutrient cycling in oligotrophic systems, but also raise important questions about whether symbiont metabolism spurs Cassiopea growth and proliferation at sites with chronic anthropogenic nutrient inputs, where higher abundances can have negative effects on local fauna and flora.

[1]  C. Layman,et al.  Comparison of zooxanthellae densities from upside-down jellyfish, Cassiopea xamachana, across coastal habitats of The Bahamas , 2016 .

[2]  Cole G Easson,et al.  Symbiont carbon and nitrogen assimilation in the Cassiopea–Symbiodinium mutualism , 2016 .

[3]  J. Houghton,et al.  Not all jellyfish are equal: isotopic evidence for inter- and intraspecific variation in jellyfish trophic ecology , 2015, PeerJ.

[4]  N. Knowlton,et al.  Productivity links morphology, symbiont specificity and bleaching in the evolution of Caribbean octocoral symbioses , 2015, The ISME Journal.

[5]  C. Layman,et al.  Bristle worms attack: benthic jellyfish are not trophic dead ends , 2015 .

[6]  Cole G Easson,et al.  Shifts in sponge-microbe mutualisms across an experimental irradiance gradient , 2015 .

[7]  C. Layman,et al.  Modification of a seagrass community by benthic jellyfish blooms and nutrient enrichment , 2014 .

[8]  R. Carmichael,et al.  Determination of δ13C and δ15N and trophic fractionation in jellyfish: implications for food web ecology , 2014 .

[9]  C. Trueman,et al.  Testing the long-term stability of marine isoscapes in shelf seas using jellyfish tissues , 2014, Biogeochemistry.

[10]  T. Filley,et al.  Land use, water quality, and the history of coral assemblages at Bocas del Toro, Panamá , 2014 .

[11]  M. Fogel,et al.  Quality or quantity: is nutrient transfer driven more by symbiont identity and productivity than by symbiont abundance? , 2013, The ISME Journal.

[12]  R. Thacker,et al.  Complex interactions between marine sponges and their symbiotic microbial communities , 2011 .

[13]  C. Layman,et al.  Effects of anthropogenic disturbance on the abundance and size of epibenthic jellyfish Cassiopea spp. , 2011, Marine pollution bulletin.

[14]  J. Weisz,et al.  Zooxanthellar Symbionts Shape Host Sponge Trophic Status Through Translocation of Carbon , 2010, The Biological Bulletin.

[15]  C. Wild,et al.  Enhanced pore-water nutrient fluxes by the upside-down jellyfish Cassiopea sp. in a Red Sea coral reef , 2010 .

[16]  T. Meziane,et al.  Oxygen and nutrient dynamics of the upside down jellyfish (Cassiopea sp.) and its influence on benthic nutrient exchanges and primary production , 2009, Hydrobiologia.

[17]  B. Lapointe,et al.  The use of delta(15)N in assessing sewage stress on coral reefs. , 2009, Marine pollution bulletin.

[18]  R. Hill,et al.  Diversity and expression of nitrogen fixation genes in bacterial symbionts of marine sponges. , 2008, Environmental microbiology.

[19]  K. Pitt,et al.  Influence of jellyfish blooms on carbon, nitrogen and phosphorus cycling and plankton production , 2008, Hydrobiologia.

[20]  P. Swart,et al.  The carbon and nitrogen isotopic values of particulate organic material from the Florida Keys: a temporal and spatial study , 2008, Coral Reefs.

[21]  B. Fry Stable Isotope Ecology , 2006 .

[22]  J. Fourqurean,et al.  Spatial and seasonal variability in elemental content, δ13C, and δ15N ofThalassia testudinum from South Florida and its implications for ecosystem studies , 2005 .

[23]  S. R. Santos,et al.  Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. , 2005, Protist.

[24]  G. Jácome,et al.  Lagoon Scale Processes in a Coastally Influenced Caribbean System: Implications for the Seagrass Thalassia testudinum , 2005 .

[25]  J. B. Rosario,et al.  The Effect of Fresh Water Runoff on the Distribution of Dissolved Inorganic Nutrients and Plankton in the Bocas del Toro Archipelago, Caribbean Panama , 2005 .

[26]  Charles H. Mazel,et al.  Discovery of Symbiotic Nitrogen-Fixing Cyanobacteria in Corals , 2004, Science.

[27]  A. Baker Flexibility and Specificity in Coral-Algal Symbiosis: Diversity, Ecology, and Biogeography of Symbiodinium , 2003 .

[28]  C. Kendall,et al.  Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur , 2003 .

[29]  R. Henry,et al.  Localization and Quantification of Carbonic Anhydrase Activity in the Symbiotic Scyphozoan Cassiopea xamachana , 2003, The Biological Bulletin.

[30]  Agaricia tenuifolia,et al.  Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs , 2002 .

[31]  H. Schwarcz,et al.  Nitrogen-15 Signals of Anthropogenic Nutrient Loading in Reef Corals , 2000 .

[32]  L. R. McCloskey,et al.  Production, respiration, and photophysiology of the mangrove jellyfish Cassiopea xamachana symbiotic with zooxanthellae: effect of jellyfish size and season , 1998 .

[33]  R. Michener Stable isotope ratios as tracers in marine aquatic food webs , 1994 .

[34]  B. Lapointe,et al.  Nutrient inputs from the watershed and coastal eutrophication in the Florida keys , 1992 .

[35]  P. Kremer,et al.  DIN, DON and P04 flux by a medusa with algal symbionts , 1992 .

[36]  B. Lapointe,et al.  A comparison of nutrient-limited productivity in macroalgae from a Caribbean barrier reef and from a mangrove ecosystem , 1987 .

[37]  C. Cutress,et al.  A new Dondice (Opisthobranchia: Favorinidae), predator of Cassiopea in southwest Puerto Rico , 1985 .

[38]  L. Muscatine,et al.  Reef Corals: Mutualistic Symbioses Adapted to Nutrient-Poor Environments , 1977 .

[39]  L. Muscatine,et al.  ASSIMILATION OF PHOTOSYNTHETIC PRODUCTS OF ZOOXANTHELLAE BY A REEF CORAL. , 1969, The Biological bulletin.