Benefit of Pulsation in Soft Corals

Benefit of pulsation in soft corals Maya Kremiena,b,1, Uri Shavitc, Tali Massa,d,e, and Amatzia Genina,e aHeinz Steinitz Marine Biology Laboratory, Interuniversity Institute for Marine Sciences, Eilat 88103, Israel; bInstitute of Earth Sciences and eDepartment of Ecology, Evolution, and Behavior, Alexander Silberman Institute of Life Sciences, Hebrew University of Jerusalem, Jerusalem 91904, Israel; cCivil and Environmental Engineering, Technion, Haifa 32000, Israel; and dInstitute of Marine and Coastal Sciences, Rutgers, State University of New Jersey, New Brunswick, NJ 08901 Edited by Tom M. Fenchel, University of Copenhagen, Helsingor, Denmark, and approved March 27, 2013 (received for review February 1, 2013) Soft corals of the family Xeniidae exhibit a unique, rhythmic CO2 binding by ribulose-1,5-bisphosphate carboxylase oxygenase pulsation of their tentacles (Movie S1), first noted by Lamarck (RuBisCO) (10), thereby increasing the rate of photosynthesis by nearly 200 y ago. However, the adaptive benefit of this perpetual, the coral’s endosymbiontic algae (9). Our study of the above pre- energetically costly motion is poorly understood. Using in situ un- dictions, including a characterization of the pulsation rhythm and derwater particle image velocimetry, we found that the pulsation its hydrodynamic effects, was carried out with the xeniid coral motions thrust water upward and enhance mixing across the Heteroxenia fuscescens (Fig. 1) from the coral reef of Eilat, coral–water boundary layer. The induced upward motion effec- Red Sea, where this and several other xeniid species are tively prevents refiltration of water by neighboring polyps, while common (10, 11). the intensification of mixing, together with the upward flow, greatly enhances the coral’s photosynthesis. A series of controlled Results laboratory experiments with the common xeniid coral Heteroxenia Pulsation Cycles. Pulsation activity during day and night was ex- fuscescens showed that the net photosynthesis rate during pulsa- amined in situ with four different H. fuscescens colonies at 5- to tion was up to an order of magnitude higher than during the 10-m depth, using an underwater infrared (IR)-sensitive video coral’s resting, nonpulsating state. This enhancement diminished camera cabled to shore. Underwater IR illumination was used when the concentration of oxygen in the ambient water was arti- during the night (Materials and Methods). The period of one full fi cially raised, indicating that the enhancement of photosynthesis pulsation cycle was on average (±SD) 1.6 s (±0.18 s) (n = 72), fl ECOLOGY was due to a greater ef ux of oxygen from the coral tissues. By with no phase synchronization among neighboring polyps within lowering the internal oxygen concentration, pulsation alleviates the colony (Fig. 1A). fi the problem of reduced af nity of ribulose-1,5-bisphosphate car- Complete diel (24-h) records obtained for three of the colo- boxylase oxygenase (RuBisCO) to CO2 under conditions of high nies showed that the corals pulsate continuously during most oxygen concentrations. The photosynthesis–respiration ratio of > – H. fuscescens ( 95%) of the time. Short (15 30 min) intervals without pulsa- the pulsating was markedly higher than the ratios tion (hereafter “rest”; Fig. 1B) were observed once a day, usually reported for nonpulsating soft and stony corals. Although pulsa- > fi in late afternoon (Fig. 2). The entire record ( 350 h) showed tion is commonly used for locomotion and ltration in marine that resting intervals always occurred when the intensity of solar mobile animals, its occurrence in sessile (bottom-attached) species radiation was <50% of the daily maximum. is limited to members of the ancient phylum Cnidaria, where it is used to accelerate water and enhance physiological processes. Pulsation, Respiration, and Photosynthesis. A comparison of respiration and photosynthesis between pulsating and resting mass balance | diffusion | mass transfer coefficient | Red Sea H. fuscescens was carried out in the laboratory with freshly col- lected colonies (Materials and Methods). As shown in Fig. 3, these unique characteristic of soft corals belonging to the family measurements indicate that the coral’s respiration rate during AXeniidae (phylum Cnidaria) is the perpetual, nonsynchro- pulsation was approximately two times higher than during rest nous pulsation of the colony’s polyps (Movie S1). This unique periods (mean ± SD =×2.06 ± 0.28), whereas the gross photo- motion, consisting of a rhythmic extension and contraction of the synthesis was sevenfold higher (×7.11 ± 0.96); Fisher’s combined tentacles, was first noted two centuries ago by Lamarck (1). probability test: P < 0.01, n = 3 measurements for each of the three However, neither its biomechanical effects nor its benefits to the colonies for each of the respiration and photosynthesis measure- coral are understood. To the best of our knowledge, no other ments. A similar pattern was found in a different experiment where ’ sessile organism in the world s oceans exhibits such a behavior. we measured the change in net photosynthesis as function of The closest motion resembling this pulsation is exhibited by me- irradiance intensity (P–I curves). The results (Fig. 4) show that in dusae that rhythmically contract their bell (exumbrella) to swim the pulsating corals the slope of the P–I curve was much steeper, (2, 3) or enhance nutrient uptake (4–6). reaching about an order of magnitude higher Pmax than in the As pulsation in xeniid corals is vigorous and perpetual, its resting corals. Here, the enhancement of photosynthesis was al- fi bene t should be considerable. Because all xeniid corals host ready noticeable at dim light (3,500 lx), equivalent to the intensity symbiotic algae, and because food particles are rarely found in of light at 10-m depth about 1 h after sunrise or before sunset. their gastrovascular cavity (7, 8), a positive effect of pulsation on During pulsation, the stems of the active polyps are always carbon acquisition via photosynthesis of their symbionts or on extended and their tentacles rhythmically change their posture the uptake of dissolved matter from the surrounding waters can from being fully extended in the open state, to being tightly be especially beneficial for these animals. Here, we measured the metabolic cost of pulsation and tested fi the hypothesis that the key bene ts of pulsation are the en- Author contributions: M.K., U.S., and A.G. designed research; M.K., U.S., T.M., and A.G. hancement of photosynthesis by the coral’s symbiotic algae and performed research; U.S. and T.M. contributed new reagents/analytic tools; M.K., U.S., the prevention of water refiltration by neighboring polyps. The and A.G. analyzed data; and M.K., U.S., and A.G. wrote the paper. proposed effect on photosynthesis is based on the prediction that The authors declare no conflict of interest. pulsation intensifies mixing and accelerates the flow over the This article is a PNAS Direct Submission. coral–water interface, which, in turn, increases the efflux of 1To whom correspondence should be addressed. E-mail: [email protected]. ’ oxygen away from the coral s tissues (9). The maintenance of low This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. concentration of oxygen inside the coral is expected to enhance 1073/pnas.1301826110/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1301826110 PNAS Early Edition | 1of6 Indeed, the increase in ambient oxygen practically eliminated the effect of pulsation on photosynthesis (Fig. 3B; Mann–Whitney, P = 0.51, n = 3 colonies, testing for a difference in gross photosynthesis between pulsation under high oxygen and rest under normal oxygen). Note that the photosynthesis rate in the nonpulsating state was unaffected by the change in ambient oxygen (Mann–Whitney, P = 0.83, n = 3). Hydrodynamic Effects of Pulsation. The flow field generated by pulsation was recorded in situ using our custom-built underwater particle image velocimetry (UPIV) system (Materials and Methods), positioned at the reef so that the measurement domain was located above the center of the coral colony (Fig. S1). Pulsation markedly changed the flow pattern above the coral polyps (Fig. S1). Most noticeable was the vertical (upward) thrust driven by pulsation near the coral–water interface (Fig. S2A): whereas during rest the vertical velocity near that interface was weaker than that measured at 1.8 cm above the coral, under pulsating state the former velocity was about twice the latter. Lagrangian simulations were used to generate particle trajectories to further explore the flow patterns generated by pulsation. To do so, imaginary particles were “released” at the coral–water interface and tracked using our UPIV time series until they exited the measurement domain (Materials and Methods). As each trajectory started at the coral surface, where waterborne commodities such as dissolved gasses and nutrients are taken up by the coral, the simulation allowed us to assess the effect of pulsation on the probability of water refiltration by neighboring polyps. The results show that pulsation substantially reduced that probability; whereas in resting corals >50% of the imaginary particles (of a total of 1,379 trajectories) were refiltered at least once (Fig. 5 B and D), less than 20% of the trajectories (of a total of 4,949) showed refiltration during pulsation (Fig. 5 A and C). Moreover, during pulsation the frequency distribution Fig. 1. The Xeniid coral Heteroxenia fuscescens during pulsation (A) and rest (B). Note the different postures of the tentacles among the pulsating polyps, demonstrating the absence of phase synchronization among the polyps within the colony. (C) A schematic illustration of the stem and tentacles of a single polyp. packed in the closed posture (Fig. 1 and Movie S1). Conse- quently, the surface area exposed to downwelling light during pulsation was on average (±SD) 2.69 (±0.26) times greater than during the resting state (n = 3).

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