Exposure to sediment enhances primary acquisition of Symbiodinium by asymbiotic coral larvae

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 Symbiodinium 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. Additionally, 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 publisherMar Ecol Prog Ser 377: [149][150][151][152][153][154][155][156] 2009 stress events such as bleaching then this mode may be advantageous in the long-term life history of the species. Furthermore, adults of some host species may be able to acquire a new strain of Symbiodinium through secondary acquisition following stress events, such as bleaching (Kinzie et al. 2001). Despite its apparent adaptive advantages, secondary acquisition in scleractinian corals has not been observed, possibly due to experimental limitations. This lack of evidence has lead investigators to suggest that hosts shuffling proportions of different Symbiodinium strains already in hospite is the predominant mode of physiological adaptation in scleractinian corals (Berkelmans & van Oppen 2006). If this is the case, then primary acquisition of Symbiodinium strains is critically important in the entire life history of these hosts. Resilience of symbiotic reef organisms, like corals, may thus be especially reliant upon the symbiont types specifically involved in primary acquisition (Baird et al. 2007).Given the dependence of reef invertebrates on environmental pools of Symbiodinium, it is imperative to understand the diversity and ecology of free-living Symbiodinium and their interactions with potential hosts. Free-living Symbiodinium have been identified in the water column...

Dispersal of Symbiodinium by the stoplight parrotfish Sparisoma viride

“…Mean densities (3207 + 1327 to 8900 + 4568 cells ml 21 ) in parrotfish faeces correlated with those identified in sediments (1000-4000 cells ml 21 ) [20], but greater concentrations (up to 38.3 Â 10 3 Symbiodinium cells ml 21 ) were identified in individual faeces samples, suggesting that fishes carry significantly higher levels of Symbiodinium and that the continuous deposition of faeces on the substrate constitutes an important source of free-living cells [17].…”

“…Successful amplifications were obtained for uncultured (17) and cultured (five) samples. However, because of sequencing limitations, only 39 sequences were recovered (see the electronic supplementary material).…”

“…Successful cultures suggested that Symbiodinium cells from faeces were alive and viable after passing through the digestive tract of the fishes. The regular presence of divergent strains of Symbiodinium clade A in cultures and fresh faeces explains why they are frequently detected in benthic environmental samples [16][17][18]. The presence of clade G in faeces was surprising, as it has only been identified as an endosymbiont of two clionaid sponges [11] and has not been detected in the environment.…”

Temperature and Water Quality-Related Patterns in Sediment-Associated Symbiodinium Communities Impact Symbiont Uptake and Fitness of Juveniles in the Genus Acropora

“…Environmental pools of Symbiodinium are thought to influence the uptake of Symbiodinium by both larvae and juvenile corals (Adams et al, 2009;Cumbo et al, 2013;Nitschke et al, 2015), although the full extent of free-living Symbiodinium diversity is uncharacterized. Heritability estimates of the Symbiodinium community in acroporid juveniles also suggest that in hospite communities are partly regulated by symbiont availability in the environmental pool and suggest that this association is flexible and adaptable (Quigley et al, 2017a,b).…”

“…Heritability estimates of the Symbiodinium community in acroporid juveniles also suggest that in hospite communities are partly regulated by symbiont availability in the environmental pool and suggest that this association is flexible and adaptable (Quigley et al, 2017a,b). For example, communities in the sediments act as a link between in hospite communities in adult corals, which continually re-seed the environmental pool, and the establishment of symbiont communities in juveniles through re-seeding from the environmental pool (Nitschke et al, 2015), and have been shown to significantly increase acquisition of Symbiodinium in larvae compared to the water column (Adams et al, 2009). However, lack of knowledge of the diversity, distribution and abundance of free-living dinoflagellates is currently limiting our understanding of environmental impacts on the establishment of coral-Symbiodinium symbioses.…”