Exposure to Sediment Enhances Primary Acquisition of Symbiodinium by Asymbiotic Coral Larvae

Vol. 377: 149–156, 2009 MARINE ECOLOGY PROGRESS SERIES Published February 26 doi: 10.3354/meps07834 Mar Ecol Prog Ser Exposure to sediment enhances primary acquisition of Symbiodinium by asymbiotic coral larvae Lisa M. Adams1,*, Vivian R. Cumbo2, Misaki Takabayashi1 1Marine Science Department, University of Hawai‘i at Hilo, 200 West Kawili St., Hilo, Hawai‘i 96720, USA 2School of Marine and Tropical Biology, James Cook University, Townsville, Queensland 4811, Australia ABSTRACT: Many symbiotic marine invertebrates acquire free-living Symbiodinium from the environment. Abundance and diversity of free-living Symbiodinium could influence recovery from bleaching, resilience, and the long-term adaptation of host organisms. Although free-living Symbio- dinium have been detected in the water column and substrates of coral reefs, their diversity and availability to the hosts are poorly understood. Tank experiments were conducted to test whether asymbiotic coral larvae of Acropora monticulosa acquired free-living Symbiodinium from the water column or sediment to become symbiotic. Treatments included filtered (0.22 µm) seawater (FSW), unfiltered seawater (SW), FSW and sediment, and SW and sediment. Our results showed that greater proportions of larvae in sediment-containing treatments acquired Symbiodinium earlier and had greater in hospite Symbiodinium densities when compared to seawater-only treatments. Addition- ally, clade A Symbiodinium was only recovered in the larvae from the sediment-containing treatments, whereas clades B and C were recovered from all treatments. Differences in distribution, abundance, replication and motility patterns of Symbiodinium, as well as larval behavior, may have contributed to the observed differences between uptake from the sediment and the water column. However, our results suggest that the sediment may represent an important source of free-living Symbiodinium available for uptake during primary acquisition by coral larvae. KEY WORDS: Free-living Symbiodinium · Acquisition · Coral larvae · Reef sediment · Water column · Acropora monticulosa Resale or republication not permitted without written consent of the publisher INTRODUCTION Symbiodinium types and/or those best adapted to the local environment (Toller et al. 2001, Berkelmans & An array of foraminiferans, mollusks, and cnidarians van Oppen 2006). benefit from mutualistic symbioses with dinoflagel- Invertebrate hosts may obtain Symbiodinium ‘verti- lates of the genus Symbiodinium, commonly known as cally,’ from parent to offspring, or ‘horizontally,’ from zooxanthellae. Genetic analyses have divided the the environment surrounding them (Harrison & Wal- genus Symbiodinium into 8 clades (A through H) and lace 1990). Horizontal acquisition is, debatably, benefi- numerous subclades and strains (Pochon et al. 2006, cial to hosts, giving each generation of hosts an oppor- Sampayo et al. 2007). The type of Symbiodinium in tunity to associate with diverse types or a particular hospite can influence the biological processes of the type of Symbiodinium that is adaptive to the local envi- invertebrate host such as growth and reproduction ronmental conditions (Buddemeier & Fautin 1993, (Kinzie & Chee 1979, Fitt 1985, Little et al. 2004). Ulti- Glynn 1993, Brown 1997, Kinzie et al. 2001, Douglas mately, the dinoflagellate symbiont plays a crucial role 2003, Fautin & Buddemeier 2004). Dominance of a new in determining the fate of the host throughout its life- symbiont type may be a disadvantage to the host, lead- time and host adaptability under variable environmen- ing to decreased health, growth or reproduction (Little tal conditions over generations. Thus the fitness of the et al. 2004, Stat et al. 2008). However if the new domi- host may be enhanced by associating with diverse nant symbiont enables survival of the host through *Email: [email protected] © Inter-Research 2009 · www.int-res.com 150 Mar Ecol Prog Ser 377: 149–156, 2009 stress events such as bleaching then this mode may be 30 min and then reared in filtered seawater (0.22 µm) advantageous in the long-term life history of the spe- until larvae were ready for transport. The 2 d old asym- cies. Furthermore, adults of some host species may be biotic larvae that were swimming and had developed a able to acquire a new strain of Symbiodinium through mouth were transported in filtered seawater (0.22 µm) secondary acquisition following stress events, such as to the Sesoko Tropical Biosphere Research Center, bleaching (Kinzie et al. 2001). Despite its apparent Okinawa, Japan. These larvae were added to experi- adaptive advantages, secondary acquisition in sclerac- mental treatments on the third day after spawning. tinian corals has not been observed, possibly due to Additionally, fragments from 10 adult colonies of A. experimental limitations. This lack of evidence has monticulosa were also collected at Sakubaru from a lead investigators to suggest that hosts shuffling pro- depth of 1 to 4 m for DNA analysis of symbiont type to portions of different Symbiodinium strains already in compare with those acquired by larvae. hospite is the predominant mode of physiological Acquisition experiment. Four treatments, each with adaptation in scleractinian corals (Berkelmans & van 3 replicates (12 aquaria total), were used to identify the Oppen 2006). If this is the case, then primary acquisi- source of Symbiodinium that were acquired by asym- tion of Symbiodinium strains is critically important in biotic Acropora monticulosa larvae in a tank experi- the entire life history of these hosts. Resilience of sym- ment: (1) filtered (0.22 µm) seawater (FSW), (2) unfil- biotic reef organisms, like corals, may thus be espe- tered seawater (SW), (3) natural sediment and filtered cially reliant upon the symbiont types specifically seawater (FSW & SED), and (4) natural sediment with involved in primary acquisition (Baird et al. 2007). unfiltered seawater (SW & SED). Seawater and sedi- Given the dependence of reef invertebrates on envi- ment used in treatment aquaria were collected from ronmental pools of Symbiodinium, it is imperative to the reef immediately south of Sesoko Station between understand the diversity and ecology of free-living 15:00 and 17:00 h on August 7, 2007 (Day 0). Surface Symbiodinium and their interactions with potential seawater was collected from directly over the reef at hosts. Free-living Symbiodinium have been identified <1 m depth. Sediment was collected using a 50 ml fal- in the water column and substrates of coral reefs con tube by gently collecting the top, oxic layer (deter- (Carlos et al. 1999, Coffroth et al. 2006, Koike et al. mined by coloration; gray or black sediment indicating 2007, Hirose et al. 2008, Littman et al. 2008, Manning & anoxic conditions) of sediment. All sediment samples Gates 2008, Porto et al. 2008). To date the diversity of were collected from the reef at the 2 to 5 m depth. free-living Symbiodinium and their availability for up- Aquaria were approximately 1.5 l in volume and con- take by host organisms have been poorly characterized. tained 1.0 l of seawater and, when appropriate, 100 ml In hospite studies have utilized settled coral recruits to of sediment. Aquaria were left alone for 6 h to allow investigate primary acquisition of Symbiodinium sediment to settle and temperatures of seawater to (Kinzie et al. 2001, Coffroth et al. 2006). However, set- equilibrate with room temperature (27°C). On Day 0, tlement materials may influence results if free-living 100 larvae were added to each aquarium. Aquaria Symbiodinium are attracted to artificial substrates. were maintained at 27°C and exposed to an average of Moreover, acquisition could occur in larvae before 60 to 80 µmol photons m–2 s–1 of light on a 12 h light: metamorphosis to the juvenile polyp stage (Schwarz et dark cycle. Gentle airflow was also applied to all al. 1999, Weis et al. 2001, RodriguezLanetty et al. 2004, aquaria, producing minimal water circulation. Marlow & Martindale 2007). In the present study, we At each census (3, 6, and 12 d after initiation), 10 larvae tested whether asymbiotic coral larvae of Acropora from each aquarium were surveyed for the presence or monticulosa preferentially acquired free-living Sym- absence of Symbiodinium. Larvae were washed in fil- biodinium from the water column or sediment. tered seawater (0.22 µm), mounted onto glass slides with cover slips, and viewed under an epifluorescent micro- scope (Nikon Microphot-FXA). With excitation of 450 to MATERIALS AND METHODS 490 nm and filter of 510 to 550 nm (B2 filter set), the larvae fluoresced green and the Symbiodinium were bright Collection. Six mature colonies of Acropora montic- red due to chlorophyll a (chl a), making the presence of ulosa were collected from the southwest side of the symbionts very easy to identify. Cover slips were placed island of Akajima at Sakubaru, Japan, and taken to the gently over the larvae, flattening without rupturing Akajima Marine Science Laboratory (AMSL). Colonies them, into a 1-dimensional plane to more accurately were maintained in tanks with running seawater until count Symbiodinium in hospite. For each larva, acquisi- spawning time, where they were isolated in an aquar- tion status (presence or absence of Symbiodinium) and ium and allowed to spawn. Spawning occurred the number of resident Symbiodinium were recorded. between 23:00 and 23:30 h on August 4, 2007. Eggs Statistical analysis. The Day 6 data were used in and sperm were collected, allowed to fertilize for statistical analysis of Symbiodinium densities because Adams et al.: Acquisition of free-living Symbiodinium from sediment 151 it was the only day that had density data for all treat- University of Hawai‘i at Manoa. A total of 19 to 25 ments, and essentially represented the end of the clones per aquarium sample and 1 to 10 clones per experiment. The filtered seawater and seawater treat- adult coral colony were sequenced. Chromatograms of ments were the only ones for which data were avail- sequenced clones were manually checked and aligned able on Day 12; both the proportion of symbiotic larvae with Sequencher 4.5 (Gene Codes).

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