Potential energetic and oxygenic benefits to unstable photosymbiosis in the cladobranch slug, Berghia stephanieae (Nudibranchia, Aeolidiidae)

ABSTRACT

Some cladobranch sea slugs host algae (Symbiodiniaceae), forming stable or unstable photosymbiotic relationships. Although some benefits from retaining symbionts have been described in stable photosymbioses, unstable photosymbioses remain largely uninvestigated. We examined two potential benefits – nutrition and oxygen produced via photosynthesis – in the unstable cladobranch model species, Berghia stephanieae. To investigate potential nutritive benefits, we conducted transmission electron microscopy and observed both partially digested symbionts and lipid droplets, indicating that B. stephanieae benefits energetically from hosting zooxanthellae through digestion. Since increased temperatures can cause oxygen limitation, any oxygenic benefits B. stephanieae receives from photosynthesis could influence their thermal tolerance, allowing photosynthetic slugs to withstand higher temperatures than specimens where photosynthesis is limited or absent. To assess this, we measured the maximum temperature they can withstand before succumbing to heat-shock under three light intensities (0, 100 and 700 µmol m^-2s^-1). Oxygen uptake was measured before and after heat-shock to determine whether uptake was affected by thermal stress. Slugs exposed to high light displayed significantly lower thermal limits than those at zero or moderate light, indicating exposure to acute high light negatively impacts thermal tolerance. Lastly, we assessed if and how light affects juvenile development and survival. Juveniles exposed to moderate light survived longest, while both other light intensities reduced survival. These investigations demonstrate that unstable photosymbiosis provides B. stephanieae with nutritive benefits during different ontogenetic stages. Oxygenic benefits are less clear, as slugs exposed to thermal stress in dark and under moderate light did not display different thermal tolerances.

KEYWORDS:

• Symbiosis
• thermal tolerance
• hyperthermal stress
• light stress
• nudibranch
• zooxanthellae

Acknowledgements

We would like to thank Can Kahyaoglu, Michiel Merkx, Maja Bošnjaković and Rianne Pap for their help throughout this project, our technicians Jan Veldsink and Stella Boele-Bos for help in the laboratory (all University of Groningen) and the staff at Frits Kuiper Aquarium store in Groningen, The Netherlands, for supplying us with anemones. We would also like to thank Jenny Melo Clavijo and Elena Garcia Galera (University of Wuppertal) for providing and fixing the tissue for TEM imaging. We also greatly appreciate Klemens Eriksson (University of Groningen) for lending us lab space and supplies. Finally, we would like to thank our editor, Dr. Carolin Löscher and an anonymous reviewer for their suggestions.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Additional information

Funding

We are grateful to the Dutch Research Council (NWO), who financed this work as part of the project VI.Veni.202.218, which was awarded to EMJL. GC was funded by the EvoSym project [grant number POCI-01-0145-FEDER-028751].