Environmental factors controlling the distribution of symbiodinium harboured by the coral Acropora millepora on the Great Barrier Reef

Abstract

Background: The Symbiodinium community associated with scleractinian corals is widely considered to be shaped by seawater temperature, as the coral's upper temperature tolerance is largely contingent on the Symbiodinium types harboured. Few studies have challenged this paradigm as knowledge of other environmental drivers on the distribution of Symbiodinium is limited. Here, we examine the influence of a range of environmental variables on the distribution of Symbiodinium associated with Acropora millepora collected from 47 coral reefs spanning 1,400 km on the Great Barrier Reef (GBR), Australia.

Methodology/principal findings: The environmental data included Moderate Resolution Imaging Spectroradiometer (MODIS) satellite data at 1 km spatial resolution from which a number of sea surface temperature (SST) and water quality metrics were derived. In addition, the carbonate and mud composition of sediments were incorporated into the analysis along with in situ water quality samples for a subset of locations. Analyses were conducted at three spatio-temporal scales [GBR (regional-scale), Whitsunday Islands (local-scale) and Keppel Islands/Trunk Reef (temporal)] to examine the effects of scale on the distribution patterns. While SST metrics were important drivers of the distribution of Symbiodinium types at regional and temporal scales, our results demonstrate that spatial variability in water quality correlates significantly with Symbiodinium distribution at local scales. Background levels of Symbiodinium types were greatest at turbid inshore locations of the Whitsunday Islands where SST predictors were not as important. This was not the case at regional scales where combinations of mud and carbonate sediment content coupled with SST anomalies and mean summer SST explained 51.3% of the variation in dominant Symbiodinium communities.

Conclusions/significance: Reef corals may respond to global-scale stressors such as climate change through changes in their resident symbiont communities, however, management of local-scale stressors such as altered water quality is also necessary for maintenance of coral-Symbiodinium associations.

Figure 1. Geographic distribution of Symbiodinium types in A. millepora on the Great Barrier Reef.

Dominant (a) and (c), and background (b) and (d) levels of Symbiodinium. Underlay for (a) and (b) is long-term mean SST (9-year; °C) and for (c) and (d) long-term mean Secchi depth (7-year; m). * indicate local-scale data points, † indicate samples included in temporal analysis. Background levels of Symbiodinium, determined based on co-occurring lower intensity bands, was detected in only 12% of samples; hence the (b) and (d) represent a smaller sample size.

Figure 2. Two-dimensional MDS plot of the Symbiodinium community sampled at each of four regions on the Great Barrier Reef.

Symbols: ▵ Far Northern, + Northern, ▪ Whitsundays, ○ Southern GBR. For symbiont types, bold indicates a dominant type and italics are those occurring at background levels.

Figure 3. Distance based redundancy ordination (dbRDA) for the fitted model of Symbiodinium communities associated with the hard coral Acropora millepora and environmental parameters for four regions of the Great Barrier Reef.

Symbols: ▵ Far Northern, + Northern, ▪ Whitsundays, ○ Southern GBR.

Figure 4. Partial plots of the GAMs of dominant Symbiodinium types along gradients of long-term SST (9-year), SST summer mean, 3-month Secchi depth, anomalies in Secchi depth, mud and carbonate content of sediments on the Great Barrier Reef.

Solid line shows the model and grey area is the 95% confidence interval. Y-axis is scaled to abundance, values around zero indicate absent symbiont type, negative units are included as they represent the range of confidence limit boundaries.

Figure 5. Two-dimensional MDS plot of the Symbiodinium community sampled at each of two water quality zones along a gradient in the Whitsunday Islands of the Great Barrier Reef.

Symbols: ▾ inner zone, ▴ outer zone. For symbiont types, bold indicates a dominant type and italics are those occurring at background levels. Locations defined as occurring in inner and outer zones of water quality using thresholds described by De'ath and Fabricius (2010) .

Figure 6. dbRDA ordination for the fitted model of Symbiodinium communities associated with the hard coral Acropora millepora and environmental parameters for two zones of water quality in the Whitsunday Islands.

Symbols: ▾ inner zone, ▴ outer zone.

Figure 7. dbRDA ordination for the fitted model of Symbiodinium communities associated with the hard coral Acropora millepora and environmental parameters for different years of sampling at Trunk Reef and the Keppel Islands.

Symbols: + Trunk Reef, ▴ North Keppel Is., ▪ Miall Is., • Halfway Is. Colours: red 2001, green 2002, black 2003, navy blue 2004, light blue 2005, pink 2006, yellow 2008, grey 2009. For symbiont types, bold indicates a dominant type and italics are those occurring in background levels.

Figure 8. SSCP gel image.

The image illustrates the link between band intensity and how relative abundance (dominant or background) of Symbiodinium strains was determined for individual samples. Samples in Bold = dominant, Bold/Normal = dominant/background, Normal/Normal = equal band intensities, Bold Italics/Normal = slight dominance/significant background.