Atypical plant–herbivore association of algal food and a kleptoplastic sea slug (Elysia clarki) revealed by DNA barcoding and field surveys
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The identity of food sources and feeding preferences of specialist herbivores have been commonly inferred from spatial associations between consumer and food items. However, such basic information for well-known marine herbivores, sacoglossans (sea slugs), and their algal diets remains disappointingly lacking, especially from field studies. The sacoglossan, Elysia clarki (Pierce et al. in Molluscan Res 26:23–38, 2006), is kleptoplastic and sequesters chloroplasts from algal food to photosynthesize, so DNA identification of sequestered chloroplasts was employed to verify the algal species fed upon by the slug across its geographic range. The molecular information on the algae consumed by E. clarki was combined with field surveys of slugs and algae in slug habitats in the Florida Keys in July and August of 2008 in order to evaluate whether the diet of this herbivore could be predicted based on its spatial association with algae in the field. A considerable mismatch between food availability and kleptoplast identity was recorded. E. clarki commonly occupied areas devoid of potential food and often contained symbiotic plastids from algal species different from those most frequently found in the surveyed habitats. In three of the four study sites, algal species present were poor predictors of slug diet. These findings suggest that the photosynthetic capability of E. clarki may release the slug from the constraint of requiring proximity to its food sources and may allow for the potential lack of spatial coupling between this herbivore and its algal food. This combination of field surveys and DNA barcoding provided critical and previously unavailable information on herbivore feeding in this marine system.
KeywordsAlgal Species Spatial Association Halimeda Online Resource Table Specialist Herbivore
Financial support for this research was provided by a Lerner Gray Fellowship and a Tharp Graduate Award, USF, to MLM, and a private donor, to SKP, who wishes to remain anonymous. Specimens were collected under permit SAL-11-0616-SR issued to SKP by the State of Florida Fish and Wildlife Conservation Commission. We thank Julie Schwartz for logistical assistance and Peter Stiling and Margaret Hall for comments on a previous version of the manuscript. We also thank the Keys Marine Lab for logistical assistance.
- Bucklin A, Steinke D, Blanco-Bercial L (2011) DNA barcoding of marine metazoa. In: Carlson CA, Giovannoni SJ (eds) Annu Rev Mar Sci, Vol 3. Annual Reviews, Palo Alto, pp 471–508Google Scholar
- Christa G, Wescott L, Schaberle TF, Konig GM, Wagele H (2013) What remains after 2 months of starvation? Analysis of sequestered algae in a photosynthetic slug, Plakobranchus ocellatus (Sacoglossa, Opisthobranchia), by barcoding. Planta 237:559–572. doi: 10.1007/s00425-012-1788-6 CrossRefGoogle Scholar
- Clark KB (1994) Ascoglossan (=sacoglossa) mollusks in the Florida Keys: rare marine invertebrates at special risk. Bull Mar Sci 54:900–916Google Scholar
- Clark KB, Jensen KR, Stirts HM (1990) Survery for functional kleptoplasty among West Atlantic ascoglossa (=sacoglossa) (Mollusca Opisthobranchia). Veliger 33:339–345Google Scholar
- Händeler K, Wägele H (2007) Preliminary study on molecular phylogeny of Sacoglossa and a compilation of their food organisms. Bonn Zool Beitr 55:231–254Google Scholar
- Jensen KR (1980) A review of sacoglossan diets with comparative notes on radular and buccal anatomy. Malacol Rev 13:55–78Google Scholar
- Maeda T, Hirose E, Chikaraishi Y, Kawato M, Takishita K, Yoshida T, Verbruggen H, Tanaka J, Shimamura S, Takaki Y, Tsuchiya M, Iwai K, Maruyama T (2012) Algivore or Phototroph? Plakobranchus ocellatus (Gastropoda) continuously acquires kleptoplasts and nutrition from multiple algal species in nature. PLoS One 7(7):e42024. doi: 10.1371/journal.pone.0042024 CrossRefGoogle Scholar
- Miller MA, Muller GC, Kravchenko VD, Junnila A, Vernon KK, Matheson CD, Hausmann A (2006) DNA-based identification of Lepidoptera larvae and plant meals from their gut contents. Russ Entomol J 15:427–432Google Scholar
- Pierce SK, Curtis NE, Massey SE, Bass AL, Karl SA, Finney CM (2006) A morphological and molecular comparison between Elysia crispata and a new species of kleptoplastic sacoglossan sea slug (Gastropoda: Opisthobranchia) from the Florida Keys, USA. Molluscan Res 26:23–38Google Scholar
- Rogers CN, De Nys R, Steinberg PD (2000) Predation on juvenile Aplysia parvula and other small anaspidean, ascoglossan, and nudibranch gastropods by pycnogonids. Veliger 43:330–337Google Scholar
- Sørensen T (1948) A method of establishing groups of equal amplitude in plant sociology based on similarity of species and its application to analyses of the vegetation on Danish commons. Biol Skr 5:1–34Google Scholar