Monitoring coral cover can describe the ecology of reef degradation, but rarely can it reveal the proximal mechanisms of change, or achieve its full potential in informing conservation actions. Describing temporal variation in Symbiodiniaceae within corals can help address these limitations, but this is rarely a research priority. Here, we augmented an ecological time series of the coral reefs of St. John, US Virgin Islands, by describing the genetic complement of symbiotic algae in common corals. Seventy-five corals from 9 species were marked and sampled in 2017, and following hurricanes in September 2017, 41% were sampled in 2018, and 72% in 2019; 28% could not be found and were assumed to have died. Symbiodiniaceae ITS2 sequencing identified 525 distinct sequences (comprising 42 ITS2 type profiles), and symbiont diversity differed among host species and individuals, but was in most cases preserved within hosts over 3 yrs that were marked by physical disturbances from major hurricanes and the onset of stony coral tissue loss disease. While changes in symbiont communities were slight and stochastic over time within colonies, variation in the dominant symbionts among colonies was observed for all host species. Together these results indicate that declining host abundances could lead to the loss of rare algal lineages that are found in a low proportion of few coral colonies left on many reefs, especially if coral declines are symbiont-specific. These findings highlight the importance of identifying Symbiodiniaceae as part of a time series of coral communities to support holistic conservation planning. Repeated sampling of tagged corals is unlikely to be viable for this purpose, because many Caribbean corals are dying before they can be sampled multiple times. Instead, random sampling of large numbers of corals may be more effective in capturing the diversity and temporal dynamics of Symbiodiniaceae metacommunities in reef corals.

Project design and field sampling

In the summer of 2017, nine scleractinian species (Table 1) from six genera were selected based on their high abundance and ecological importance. A total of 75 coral colonies were sampled from 7–10 m depth at White Point, East Tektite, and Cabritte Horn [Fig. S1]), where the reefs have been monitored since 1992 (Edmunds 2018). Colonies were haphazardly selected along 40-m transects at each monitoring site (Edmunds 2018) between 27 July and 7 August 2017, and their positions were identified using cartesian coordinates. They were selected based on ease of location, and size (> 20-cm diameter to support multiple samplings), and marked with aluminum tags epoxied to the substratum. Following tagging, a tissue biopsy (< 1-cm diameter) was removed from the upper surface of each colony using stainless steel clippers. Samples were placed in Whirl-Pak bags and processed within 2 hours of sampling.

We searched for the tagged colonies in 2018 (13–15 August), 11 months after Hurricanes Irma and Maria, and in 2019 (24–29 July). Colonies were located using an underwater metal detector (Vibraprobe 580, Treasure Products, CA) to find their tags, underwater maps, and site photographs. When located, a tissue biopsy was collected using the identical procedure established in 2017. Sampling in 2018 was limited due to the lingering effects of the hurricanes on island infrastructure. Sampling was comprehensive in 2019, and the reefs were exhaustively searched for tagged colonies to increase confidence that missing colonies were dead rather than not located. These collections were completed under permits issued by the Virgin Islands National Park (VIIS-2017-SCI-0037, VIIS-2018-SCI-0019, VIIS-2019-SCI-0023) and the Government of the Virgin Islands (DFW18088J, DFW19044J).

DNA extraction and sequencing

On shore, coral biopsies were individually transferred to microcentrifuge tubes filled with 500 µL of 1% sodium dodecyl sulfate DNA buffer using sterilized forceps, and heated to 65°C for 1.5h. Samples were shipped to the Hawaiʻi Institute of Marine Biology where genomic DNA was extracted using an organic extraction protocol (Baker & Cunning 2016). Symbiodiniaceae diversity was characterized through the amplification and sequencing of the ribosomal Internal Transcribed Spacer 2 (ITS2) region (LaJeunesse 2001; Davies et al. 2022). DNA samples were sent to the University of Texas at Austin for library preparation with ʻitsDʻ and ʻits2rev2ʻ primers (Stat et al. 2009) and sequencing on an Illumina MiSeq platform with 2 x 300 paired-end read chemistry. The paired forward and reverse reads from each sample were submitted to SymPortal to resolve ITS2 type profiles based on repeated co-occurrence of purported intragenomic variants (Hume et al. 2019).