Foraging Behavior under Starvation Conditions Is Altered via Photosynthesis by the Marine Gastropod, Elysia clarki

Abstract

It has been well documented that nutritional state can influence the foraging behavior of animals. However, photosynthetic animals, those capable of both heterotrophy and symbiotic photosynthesis, may have a delayed behavioral response due to their ability to photosynthesize. To test this hypothesis we subjected groups of the kleptoplastic sea slug, Elysia clarki, to a gradient of starvation treatments of 4, 8, and 12 weeks plus a satiated control. Compared to the control group, slugs starved 8 and 12 weeks displayed a significant increase in the proportion of slugs feeding and a significant decrease in photosynthetic capability, as measured in maximum quantum yield and [chl a]. The 4 week group, however, showed no significant difference in feeding behavior or in the metrics of photosynthesis compared to the control. This suggests that photosynthesis in E. clarki, thought to be linked to horizontally-transferred algal genes, delays a behavioral response to starvation. This is the first demonstration of a link between photosynthetic capability in an animal and a modification of foraging behavior under conditions of starvation.

Plastid-bearing sea slugs fix CO2in the light but do not require photosynthesis to survive

“…A number of other studies also reported the incorporation of 14 C from 14 CO 2 in plakobranchids that sequester plastids [30][31][32][33], but animals can also incorporate CO 2 via carboxylation reactions. The second line of evidence for plakobranchids being photosynthetic comes from the observation that once the plastids have been incorporated into the digestive gland, LtR species can survive for months in the absence of additional food [7,10,23,24,34,35]. Such plakobranchids are said to be 'starved' and are typically cultivated in the light [8,9].…”

FISH Labeling Reveals a Horizontally Transferred Algal (Vaucheria litorea) Nuclear Gene on a Sea Slug (Elysia chlorotica) Chromosome

“…Scale bar ϭ 20 m. san species with similar lengths of plastid function longevity as E. timida (2-4 mon; namely E. viridis, E. clarki) show a variety of specific adaptations in their cell biology to sustain the function of the algal organelle. In some cases, such as E. clarki, plastid maintenance mechanisms are sufficient to enable enough photosynthesis to occur for long enough to permit some independence from a food source (Middlebrooks et al, 2011(Middlebrooks et al, , 2012(Middlebrooks et al, , 2014. Although a few recent accounts based on E. timida have discounted the importance of photosynthetic function as well as the longevity and integration of symbiotic plastid function among the sacoglossans as a group (Wägele et al, 2011;Christa et al, 2013), it is clear that the broad differences in the adaptations among species makes generalizations based on one slug species unwarranted.…”

Sacoglossan sea slugs make routine use of photosynthesis by a variety of species‐specific adaptations

“…C. Transmission electron micrograph showing kleptoplasts within the cells of a digestive tubule cul‐de‐sac (from Middlebrooks et al. ). D. Elysia chlorotica (Type 4) from Menemsha, Massachusetts are even more uniformly green than E. clarki and cannot be anatomically shaded from exposure to sunlight (photo by P. Krug).…”

“…In these species, the chloroplasts merely photosynthesize until they burn out, using up whatever algal‐originated material was engulfed initially, so that chloroplasts must be replaced by continuous feeding by the slugs (reviewed in Middlebrooks et al. , ; Pierce & Curtis ; Curtis et al. ).…”

“…In addition, E. clarki is less likely to feed when sequestered chloroplasts are fully functional, but increases feeding behavior as photosynthetic activity declines during starvation (Middlebrooks et al. ).…”