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Foraging behavior under starvation conditions is altered via photosynthesis by the marine gastropod, Elysia clarki.

Middlebrooks ML, Pierce SK, Bell SS - PLoS ONE (2011)

Bottom Line: However, photosynthetic animals, those capable of both heterotrophy and symbiotic photosynthesis, may have a delayed behavioral response due to their ability to photosynthesize.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Integrative Biology, University of South Florida, Tampa, Florida, United States of America. mlmiddle@mail.usf.edu

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.

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Electron micrograph of a digestive tubule cell of E. clarki.The digestive tubule cell is densely packed with sequestered chloroplasts. C = chloroplast, N = nucleus. Scale bar represents 3 µm. Image taken by Nicholas Curtis.
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pone-0022162-g001: Electron micrograph of a digestive tubule cell of E. clarki.The digestive tubule cell is densely packed with sequestered chloroplasts. C = chloroplast, N = nucleus. Scale bar represents 3 µm. Image taken by Nicholas Curtis.

Mentions: Most animal species capable of utilizing photosynthesis as an energy source are aquatic and sessile (e.g. corals, sponges, giant clams) or have limited motility (e.g. benthic jellyfish), and thereby do not forage at all [12]. However, the sacoglossan (Opisthobranchia: Mollusca) sea slugs are highly motile and actively forage on algae, which is usually siphonaceous and typically found in shallow water [18]. Importantly, many sacoglossans are capable of kleptoplasty, a process by which slugs photosynthesize using chloroplasts which are sequestered from the algal food by specialized cells of the digestive tubules (Figure 1) [13], [18], [19], [20]. Nuclear genes horizontally transferred from algae into the slugs likely play an important role in the slugs' ability to photosynthesize [21], [22]. These combined features suggest that kleptoplastic sea slugs are a specialized group of herbivores which can be utilized to examine how the level of satiation/starvation affects foraging behavior in a photosynthetic animal. Although increased foraging efforts under starvation conditions and a decrease during satiation is usual for many species [2], [5], the foraging behavior of photosynthetic sea slugs may be different, if food is withheld, provided that photosynthesis continues.


Foraging behavior under starvation conditions is altered via photosynthesis by the marine gastropod, Elysia clarki.

Middlebrooks ML, Pierce SK, Bell SS - PLoS ONE (2011)

Electron micrograph of a digestive tubule cell of E. clarki.The digestive tubule cell is densely packed with sequestered chloroplasts. C = chloroplast, N = nucleus. Scale bar represents 3 µm. Image taken by Nicholas Curtis.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3140505&req=5

pone-0022162-g001: Electron micrograph of a digestive tubule cell of E. clarki.The digestive tubule cell is densely packed with sequestered chloroplasts. C = chloroplast, N = nucleus. Scale bar represents 3 µm. Image taken by Nicholas Curtis.
Mentions: Most animal species capable of utilizing photosynthesis as an energy source are aquatic and sessile (e.g. corals, sponges, giant clams) or have limited motility (e.g. benthic jellyfish), and thereby do not forage at all [12]. However, the sacoglossan (Opisthobranchia: Mollusca) sea slugs are highly motile and actively forage on algae, which is usually siphonaceous and typically found in shallow water [18]. Importantly, many sacoglossans are capable of kleptoplasty, a process by which slugs photosynthesize using chloroplasts which are sequestered from the algal food by specialized cells of the digestive tubules (Figure 1) [13], [18], [19], [20]. Nuclear genes horizontally transferred from algae into the slugs likely play an important role in the slugs' ability to photosynthesize [21], [22]. These combined features suggest that kleptoplastic sea slugs are a specialized group of herbivores which can be utilized to examine how the level of satiation/starvation affects foraging behavior in a photosynthetic animal. Although increased foraging efforts under starvation conditions and a decrease during satiation is usual for many species [2], [5], the foraging behavior of photosynthetic sea slugs may be different, if food is withheld, provided that photosynthesis continues.

Bottom Line: However, photosynthetic animals, those capable of both heterotrophy and symbiotic photosynthesis, may have a delayed behavioral response due to their ability to photosynthesize.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Integrative Biology, University of South Florida, Tampa, Florida, United States of America. mlmiddle@mail.usf.edu

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.

Show MeSH
Related in: MedlinePlus