Prey species and abundance affect growth and photosynthetic performance of the polyphagous sea slug Elysia crispata

Abstract

Some sacoglossan sea slugs steal functional macroalgal chloroplasts (kleptoplasts). In this study, we investigated the effects of algal prey species and abundance on the growth and photosynthetic capacity of the tropical polyphagous sea slug Elysia crispata. Recently hatched sea slugs fed and acquired chloroplasts from the macroalga Bryopsis plumosa, but not from Acetabularia acetabulum. However, adult sea slugs were able to switch diet to A. acetabulum, rapidly replacing the great majority of the original kleptoplasts. When fed with B. plumosa, higher feeding frequency resulted in significantly higher growth and kleptoplast photosynthetic yield, as well as a slower relative decrease in these parameters upon starvation. Longevity of A. acetabulum-derived chloroplasts in E. crispata was over twofold that of B. plumosa. Furthermore, significantly lower relative weight loss under starvation was observed in sea slugs previously fed on A. acetabulum than on B. plumosa. This study shows that functionality and longevity of kleptoplasts in photosynthetic sea slugs depend on the origin of the plastids. Furthermore, we have identified A. acetabulum as a donor of photosynthetically efficient chloroplasts common to highly specialized monophagous and polyphagous sea slugs capable of long-term retention, which opens new experimental routes to unravel the unsolved mysteries of kleptoplasty.

Keywords: Acetabularia acetabulum; Bryopsis plumosa; Sacoglossa; chloroplast; kleptoplast retention time; starvation tolerance.

Figure 1.

Recently hatched E. crispata before feeding (a) and while feeding on the macroalga B. plumosa (b) from which they steal functional chloroplasts (kleptoplasts). Upon hatching, sea slugs were unable to feed directly on the macroalga A. acetabulum. However, three-month-old sea slugs feeding on B. plumosa (c) were able to switch diet to A. acetabulum, replacing the original chloroplasts within 5–10 days (d). Photo (a) was taken in an inverted microscope (DMi1, Leica Microsystems, Wetzlar, Germany), while (b), (c) and (d) were obtained using a digital microscope (DMS-300, Leica Microsystems). Scale bars represent 250 µm in (a) and (b) and 2 mm in (c) and (d).

Figure 2.

HPLC chromatograms (440 nm) showing the photosynthetic pigment composition of E. crispata fed with the macroalga B. plumosa (Ec Bp, blue line) and after 10 days feeding on the macroalga A. acetabulum (Ec Aa, red line). Pigments in blue are exclusive to B. plumosa kleptoplasts, while pigments in red are exclusive to A. acetabulum kleptoplasts. Pigments in black are common to the chloroplasts of both algae. Siph: siphonoxanthin; t-Neo: trans-neoxanthin; c-Neo: cis-neoxanthin; Viola: violaxanthin; Lut: lutein; Siph-do: siphonaxanthin dodecenoate; Chl b: chlorophyll b; Chl b ep: epimer of chlorophyll b; Chl a: chlorophyll a; Chl a ep: epimer of chlorophyll a; βε-Car: β,ε-carotene; ββ-Car: β,β-carotene.

Figure 3.

Changes in E. crispata fresh weight with feeding time and under different feeding conditions with the macroalga B. plumosa: sea slugs fed every 2 days, once per week or once every 2 weeks. Data are average ± standard deviation (n = 10 per treatment).

Figure 4.

Maximum photosynthetic yield (F_v/F_m) of E. crispata under different feeding conditions with the macroalga B. plumosa: sea slugs fed every 2 days, once per week or once every two weeks. F_v/F_m was measured at the beginning of the experiment (day 0) and at day 56, immediately before feeding. Fv/Fm was measured again 2 days after macroalgal food was provided to all the sea slugs (day 58). The line is the median, top and bottom of the box are the 75% and 25% percentiles, respectively, and the whiskers represent the maximum and minimum values (n = 10 per treatment). Outliers represented as black dots. * and *** indicate significant differences at p < 0.05 and p < 0.001, respectively.

Figure 5.

Changes in relative fresh weight of E. crispata under starvation, previously fed differently with the macroalga B. plumosa: sea slugs fed every 2 days, once per week or once every two weeks. Data are average ± standard deviation (n = 10 per treatment). Dotted lines represent linear regressions to the data (slopes: −0.0131, −0.0157 and −0.0182; r²: 0.9677, 0.9782, 0.9512, respectively).

Figure 6.

Changes in maximum photosynthetic yield (relative F_v/F_m) of E. crispata under starvation, previously fed differently with the macroalga B. plumosa: sea slugs fed every 2 days, once per week or once every two weeks. Data are average ± standard deviation (n = 10 per treatment).

Figure 7.

Changes in E. crispata fresh weight and maximum photosynthetic yield (Fv/Fm) of sea slugs under starvation, previously fed with the macroalga A. acetabulum. Data are average ± standard deviation (n = 10).

Figure 8.

Daily relative loss of fresh weight and maximum photosynthetic yield (F_v/F_m) of the sea slug E. crispata during starvation, previously fed with the macroalgae B. plumosa (Ec Bp) or A. acetabulum (Ec Aa). The line is the median, top and bottom of the box are the 75% and 25% percentiles, respectively, and the whiskers represent the maximum and minimum values (n = 10 per treatment). Outliers represented as black dots. *** indicates significant differences at p < 0.001.