Abstract
AbstractThe sacoglossan sea slug Plakobranchus ocellatus is a pantropical gastropod that pilfers and incorporates algal chloroplasts (kleptoplasts) into its digestive cells and benefits from the production of photosynthate. It is a mobile, reef forager with mottled, wing-like parapodia that provide good camouflage in sand and are typically observed closed over the kleptoplast-filled digestive tubules. Functional kleptoplasts continue to photosynthesize but are separated from the algal nuclei and are unable to divide within host cells. The mechanisms that enable kleptoplasts to endure are poorly understood and the extent and limitations of functionality have not yet been fully characterized. We investigated kleptoplasts in three tropical sacoglossan species, Elysia ornata, Thuridilla gracilis, and P. ocellatus, collected from different depths and light fields to identify pigments, quantify retention times, and determine photosynthetic parameters. We found that P. ocellatus had the highest estimated retention time and maintained the highest ratio of photoprotective to photosynthetic pigments. A subsequent manipulative experiment on P. ocellatus specimens collected at the same site, depth, and time involved exposure to three different irradiances and showed that kleptoplasts did not photoacclimate over the course of 7 d. No significant changes in in vivo kleptoplast photosynthetic parameters or corresponding spectral reflectance occurred when measuring kleptoplasts directly with open parapodia. Reflectance of closed parapodia, however, showed significant increases in the medium- and high-light treatments on day seven indicating localized kleptoplast degradation. Our results suggest that closed parapodia play an important role in kleptoplast protection by shielding internal kleptoplasts while permitting filtered light energy to reach kleptoplasts on the parapodial undersides. The cryptically patterned parapodia assume the role of photoprotectant, compensating for kleptoplast inability to photoacclimate. This allows P. ocellatus to forage in high-light, exposed, sandy areas and exploit algal food resources that may be unavailable or too risky for other sacoglossans.
Highlights
Sacoglossan gastropods (Mollusca, Opisthobranchia) are suctorial marine herbivores that remove functional chloroplasts from a variety of algal food sources (Christa et al 2014; Wade and Sherwood 2017) and relocate them to digestive cells without digestion
Previous investigations on the retention of functional chloroplasts (RFC) in sacoglossans estimated that kleptoplasts remain in hospite and functional for periods ranging from 1 h to over 3 months (Evertsen et al 2007; Pierce et al 2015)
During initial mensurative studies conducted at Lizard Island Research Station, Great Barrier Reef, Australia (LIRS; 14°40S, 145°28E), we identified the constitutive pigments in kleptoplasts and measured in vivo photosynthetic function over time to determine host RFC levels in three tropical sacoglossan species Plakobranchus ocellatus and Thuridilla gracilis (Risbec 1928), which are rarely observed with kleptoplasts exposed, and Elysia ornata (Swainson 1840; Fig. 1)
Summary
Sacoglossan gastropods (Mollusca, Opisthobranchia) are suctorial marine herbivores that remove functional chloroplasts from a variety of algal food sources (Christa et al 2014; Wade and Sherwood 2017) and relocate them to digestive cells without digestion. This remarkable ability (Handeler et al 2009; Raven et al 2009) permits the sea slugs to utilize the photosynthate produced by the stolen chloroplasts (‘‘kleptoplasts’’) to fuel their own metabolism (Trench et al 1969; Cruz et al 2020). Previous investigations on the retention of functional chloroplasts (RFC) in sacoglossans estimated that kleptoplasts remain in hospite and functional for periods ranging from 1 h to over 3 months (Evertsen et al 2007; Pierce et al 2015). Nor do we have a good understanding of the ecological importance of kleptoplasts in sacoglossans, the drivers that determine sacoglossan foraging preferences, or their abilities to travel between different light intensity regimes
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