Coral Reefs

, Volume 38, Issue 4, pp 669–676 | Cite as

A tropical Australian refuge for photosymbiotic benthic fauna

  • Zoe T. RichardsEmail author
  • Rodrigo Garcia
  • Glenn Moore
  • Jane Fromont
  • Lisa Kirkendale
  • Monika Bryce
  • Clay Bryce
  • Ana Hara
  • Jenelle Ritchie
  • Oliver Gomez
  • Corey Whisson
  • Mark Allen
  • Nerida G. Wilson


An anomalous El Niño-associated sea surface temperature stress event was predicted to affect tropical Australian reefs, including those in North Western Australia in the summer of 2015/2016. Thermal stress events are well known to result in widespread hard coral mortality events, but other symbiotic organisms such as soft corals, giant clams and sponges can also be affected. Here, we examine whether the 2016 thermal stress event deleteriously impacted coral reef communities in the remote Bonaparte Archipelago, central inshore Kimberley bioregion, North West Australia. Our results confirm the region experienced a thermal stress event of similar magnitude to other regional localities (i.e., southern Kimberley and Scott Reef), but contrary to those locations that experienced widespread bleaching events, we find no evidence to suggest widespread mortality events occurred among photosymbiotic organisms in the Bonaparte Archipelago. Photosymbiotic organisms in this region are assumed to be well adapted to fluctuating environmental conditions; however, in this instance, a greater magnitude of night-time cooling may have driven variability in regional susceptibility to thermal stress. The Bonaparte Archipelago is emerging as a globally significant ecological refuge for photosymbiotic benthic fauna that are threatened by cumulative anthropogenic and climate stressors in other parts of their distribution.


Biodiversity Coral bleaching Kimberley Scleractinia Thermal stress North West Australia 


In 2015/2016, anomalous sea temperatures associated with the El Niño period triggered a pan-tropical episode of coral bleaching (Hughes et al. 2017). Many reef systems were affected including the Hawaiian Archipelago, Fiji, New Caledonia, the Great Barrier Reef and the Maldives (Normile 2016). The impact of the coral bleaching event was well documented at some places (DeCarlo et al. 2017; Hughes et al. 2017), including many parts of Western Australia (Gilmour et al. 2019). However, at more remote locations, such as the central inshore Kimberley, North West Australia, the impact of the thermal stress event was not documented even though the region was predicted to experience up to 11 maximum degree heating weeks from February to April 2016 (Fig. 1a).
Fig. 1

a Regional time series of maximum monthly mean sea surface temperatures in North Western Australia reported from January 2015 to December 2016, showing SST that surpassed the bleaching threshold for several consecutive weeks between February and April 2016. This led to a level-2 alert being issued from March to May, meaning that widespread coral bleaching and significant coral mortality were likely (Downloaded from NOAA b Stations surveyed in this study (black triangles)

The inshore Kimberley is an unusual and dynamic tropical coral reef system. It features a semi-diurnal macrotidal regime oscillating up to 11 m, resulting in high-velocity tidally driven currents, and extremely dynamic suspended sediment loads (Wilson 2013, 2014). Over spring low tides, the intertidal communities can be exposed to ambient air temperatures and high light/UV levels for up to 3.5 h at a time (Rosser and Veron 2011; Richards et al. 2015). Across the Kimberley, the reef system is heterogeneous with distinct inshore–offshore, intertidal–subtidal and subregional patterns of community structure (Richards et al. 2018). Generally, inshore communities are dominated by hard coral (24.45% ± 1.78% percent cover), but turf and macroalgae are also major contributors to benthic cover (Richards et al. 2018). Overall, the unusual setting, low level of anthropogenic stressors and high level of coral diversity, has led the inshore Kimberley reefs to be described as important parts of Australia’s reefscape (Richards et al. 2014, 2015, 2018).

Based on published data, the central inshore Kimberley, and more specifically, a cluster of fringing and platform reefs in the Bonaparte Archipelago, appears to host the most diverse intertidal coral communities in tropical Australia. To date, 225 species of scleractinian coral have been recorded from the intertidal zone in the Bonaparte Archipelago (Richards et al. 2015). The Archipelago falls within the newly designated North Kimberley Marine Park (DPaW 2016) and the Wanjina Wunggurr Uunguu Determination Area. However, indigenous land-use agreements for the intertidal zones are not yet ratified, and there is no formal monitoring program to document the health and status of inshore Kimberley reefs. Despite routine exposure to extreme environmental conditions prior to the 2016 thermal stress event, the inshore Kimberley coral communities in the Bonaparte Archipelago and across the wider Kimberley were described as healthy (Wilson et al. 2011; Richards et al. 2015). There is no quantitative or anecdotal evidence to suggest that historical bleaching events have occurred in the Kimberley (Le Nohaïc et al. 2017). Nevertheless, no formal long-term monitoring programs monitor reef condition in the Bonaparte Archipelago; hence, the Western Australian Museum conducted a reactive reef health survey in September 2016 in response to the predicted 2016 global bleaching event.

Here, we summarize the findings of that survey which sought to examine the diversity and status of scleractinian corals and other photosymbiotic organisms (soft corals, molluscs, sponges) to determine whether they were impacted by the 2016 El Niño thermal stress event. We examine whether SST at our study site deviated during the 2016 thermal stress event from the normal temperature regime and quantify whether a higher level of cloud cover explains any observed spatial variability in susceptibility to thermal stress. This study contributes to current efforts to identify refugia (sites in which biota retreat, persist in and potentially expand from under changing environmental conditions, Keppel et al. 2012; Keppel and Wardell-Johnson 2012), and fills knowledge gaps about the biodiversity and health of intertidal and subtidal communities in the North Kimberley Marine Park.


Intertidal and subtidal surveys were conducted at 11 sites within the Bonaparte Archipelago at two platform reefs and five fringing reefs from September 16 to 21, 2016 (Fig. 1b, Table S1). Historically, these sites have been referred to as station numbers, for example 182 (Richards et al. 2018), and we will follow that approach in this manuscript. Subtidal sites were surveyed on SCUBA at 12 m depth. Mid-to-lower littoral reef flats were surveyed by reef walking at low tide. At each site, the percent cover of 12 categories of benthos (hard coral, soft coral, sponge, macroalgae, algal turf, coralline algae, calcareous algae, seagrass, other invertebrates, sand, rubble, rock and silt) was examined in situ along three 25-m point-intercept transects (50 points per transect), which were laid in a series within the same depth range. Along the first 15 m of each transect, the diversity, abundance and health of photosymbiotic organisms (i.e., hard corals, soft corals, giant clams and sponges) were documented on 1-m-wide belt transects. Comparable benthic cover estimates were obtained at four of the current survey stations in 2012 as part of WAM Woodside Collection Project (Bryce et al. 2018; Richards et al. 2018) enabling a site-specific temporal comparison.

Given the survey was undertaken approximately 6 months after the thermal stress event, it is possible that bleached white corals might not be apparent because after death, hard corals quickly become overgrown by filamentous, turf and coralline algae. Nevertheless, in a low-wave energy region such as the inshore central Kimberley, if there had been a recent widespread coral mortality event we would expect to observe dead corals in situ along with a decrease in live hard coral cover, and/or an increase in turf algal cover. To test these hypotheses, we compared the level of benthic cover in September 2016 with the dataset obtained in October 2012 using PERMANOVA with 9999 permutations in PRIMER-E (Anderson et al. 2015). A SIMPER analysis was conducted in PRIMER-E to examine the average similarity between 2012 and 2016 datasets and identify the principal drivers of dissimilarity.

To examine the normal temperature regime at our study site and quantify whether SST deviated during the 2016 thermal stress event, all available day- and night-time sea surface temperature (SST) imagery derived from MODIS Aqua, MODIS Terra and VIIRs for the Kimberley region between February and April 2011–2016, were downloaded from These data were then mapped with a cylindrical equidistant projection with the SeaDAS v7.5.1 software. The resultant SST maps had a spatial resolution native to their satellite sensor (1 km and 0.75 km for MODIS and VIIRs, respectively). For each SST image, the day- and night-time mean and standard deviation for Bonaparte Archipelago (− 14.4737 N/ 124.9794 E), southern Scott Reef (− 14.1871 N/ 121.8366 E) and Shenton Bluff (− 16.4895 N/ 123.0537 E) were calculated.

Scott Reef and Shenton Bluff were included as comparison sites because specific bleaching events were recorded at these locations (Hughes et al. 2017; Le Nohaïc et al. 2017). Shenton Bluff features a fringing reef system that occurs approximately 800 m from the mainland in the eastern edge of Cape Leveque in Western Australia. Scott Reef is an offshore Atoll reef system that occurs approximately 300 km northwest of Cape Leveque. Only pixels flagged as being of the highest quality (using the SST quality flags provided with the MODIS/VIIRs imagery) with SST temperatures > 20 °C and that were inside a site-specific polygon region-of-interest (see Fig. S1) were used. Following this initial quality control measure, a three-point boxcar average was then applied on the remaining data points to smooth out any SST values that may have been partially affected by cloud cover.

To explore the percentage of the regions of interest that were covered in cloud over the 2016 thermal stress event, Level-2 cloud mask 1 km data contained in the MOD06_L2 and MYD06_L2 products derived from MODIS’s Terra and Aqua satellites, respectively, were downloaded from for all swaths captured over the Kimberley region, North Western Australia, between February and April 2016. SeaDAS v7.5.1 was used to map all Level-2 swath image data to a common grid using cylindrical equidistant projection. Mapped image data that formed consecutive 5-min granules over the Kimberley region were mosaicked to form one image. This process generated a single mapped cloud mask image per sensor per day with a spatial resolution of 1 km. The Cloud Fraction, %, was computed for each region-of-interest (ROI) by dividing the number of cloud pixels present in the ROI by the total number of pixels in the ROI. The monthly Cloud Fraction for each ROI was then computed from the resultant MODIS time series data.

Results and discussion

By comparing the mean day- and night-time SST in February, March and April 2016 with that from 2011 to 2015 (hereafter referred to as normal), we found that higher-than-normal temperatures were experienced during the day and night within all three regions of interest in 2016 (Fig. 2, Table S2). The greatest deviations from normal occurred in April 2016, where day-time temperatures exceeded the normal by (1.17 ± 0.10) °C (Bonaparte Archipelago), (1.27 ± 0.13) °C (Scott Reef) and (1.03 ± 0.13) °C (Shenton Bluff). Similarly, night-time temperatures were (1.17 ± 0.09) °C (Bonaparte Archipelago), (1.4 ± 0.12) °C (Scott Reef) and (0.96 ± 0.10) °C (Shenton Bluff) greater than normal. All three regions experienced approximately 25 consecutive days where day-time and night-time temperatures were greater than the February–April 2016 mean, suggesting a prolonged period of sustained day- and night-time thermal stress (Fig. 2).
Fig. 2

The day-time (left column) and night-time (right column) SST at a Bonaparte Archipelago, b Scott Reef and c Shenton Bluff for the months of February to April 2016. The mean and the standard deviation for 2016 at each location are provided within the brackets. For example, the day-time mean and standard deviation for Bonaparte Archipelago between February and April 2016 were (31.07 ± 0.57) °C. This mean is also displayed as the black dashed line. Overlaid on each plot is a shaded gray region that represents one standard deviation either side of the mean SST (dark gray dotted line), which were derived from February to April 2011 to 2015 (i.e., the normal temperature regime)

Contrary to Scott Reef (Hughes et al. 2017) and Shenton Bluff (aka Shell Island, Le Nohaïc et al. 2017) where significant coral bleaching and mortality events occurred as a consequence of the 2016 thermal stress event, we found no evidence that the 2016 thermal stress event led to bleaching-induced mortality of photosymbiotic organisms in the Bonaparte Archipelago. There was no evidence of freshly dead (white) coral on the point-intercept transects, nor an increased incidence of recently dead coral that was covered in turf or filamentous algae. No hard or soft corals were pale or discolored, nor did they have visible white areas or signs of tissue loss (Fig. 3, S2–S4). Furthermore, all small-bodied giant clams had dark-brown mantles, indicative of a large number of Symbiodinium photosymbionts (Fig. 3e) and all sponges had normal coloration and appeared disease free.
Fig. 3

Healthy communities of photosymbiotic benthic fauna in the Bonaparte Archipelago. a NW Patricia Island in October 2012; b NW Patricia Island in September 2016. cPteraeolidia semperi a photosymbiotic nudibranch, dTridacna squamosa with large flutes on the shell and striped mantle; eTridacna maxima the elongate giant clam exhibiting dark-brown mantle coloration across sites; fSinularia brassica (Alcyoniidae); gKlyxum sp. which is a phototrophic soft coral that is naturally white or pale; hCliona orientalis a photosymbiotic sponge

If the thermal stress event had impacted the Bonaparte Archipelago reef community, we would expect to find a reduction in the cover of obligate photosymbiotic host taxa, especially hard corals. A PERMANOVA analysis showed the benthic community composition was significantly different between 2012 (23.65 ± 3.67%) and 2016 (36.58 ± 3.94%) (pseudo-F = 4.327, P = 0.002). This result, however, was driven by the finding of higher, not lower, coral cover in 2016 (Fig. 4a, b; SIMPER analysis, Table S3). Moreover, if coral mortality occurred as a consequence of the thermal stress event, an increase in the level of turf algae enveloping the dead coral skeletons would be expected (Diaz-Pulido and McCook 2002). However, we found the level of turf algae recorded in 2016 was not significantly different to that in 2012 (t = 0.692, df = 3, P = 0.539, see also Fig. 4c). Collectively, these results, although limited in power, provide no evidence to suggest the coral reef communities of the Bonaparte Archipelago experienced a widespread mortality event in response to the thermal stress event that impacted the region in 2016. Although we cannot unequivocally say that the photosymbiotic benthic fauna did not bleach, if they did, photosymbiotic taxa recovered their symbionts and regained color before our surveys in September 2016.
Fig. 4

Temporal change in mean percent cover of benthic organisms between 2012 and 2016 in the Bonaparte Archipelago. a Mean percent cover of biotic categories recorded at a regional scale (central inshore Kimberley) in 2012 and 2016; b mean percent cover of hard corals at four comparable stations between 2012 and 2016; c mean percent cover of turf algae at four comparable stations between 2020 and 2016

When bleaching was first reported from the inshore Kimberley (Le Nohaïc et al. 2017) and Scott Reef (Hughes et al. 2017), it was reported as being widespread in the region. Instead, our results suggest that bleaching was likely to have been patchy across the inshore Kimberley. The SST analysis we have conducted here suggests that night-time cooling may help explain the spatially variable response to the 2016 anomalous SST event. In 2016, the Bonaparte region overall experienced a (0.59 ± 0.08) °C decrease in the SST at night, which is similar to the normal level (2011–2015) of night-time cooling experienced in this region (0.57 ± 0.11) °C (see Table S2). Contrary to this, Scott Reef and Shenton Bluff had consistently lower-than-normal night-time SST resulting in lower cooling at night over these three months (Table S2). In fact in March 2016, Shenton Bluff experienced, on average, greater SST at night than during the day, though the reasons for this are presently unknown. Mechanisms that alleviate heat stress include cyclones, air–sea fluxes and internal circulation (Green et al. 2019) including strong tidal mixing (Cresswell and Babcock 2000). Our data indicate the magnitude of night-time cooling may have provided a reprieve to thermal stress in the Bonaparte Archipelago, but our regions of interest are oceanographically complex and this hypothesis requires further validation with in situ temperature data and hydrodynamic modeling.

Additional physical explanations for the spatial differences in community responses to bleaching may also relate to the finding that both the Scott Reef and Shenton Bluff communities were pre-stressed by a spate of above-normal day and night temperatures (in mid-late February and early March), whereas temperatures in the Bonaparte Archipelago remained within the range of normal variation from 2011 to 2015 over that time (Fig. 2). Furthermore, Scott Reef appears to have experienced a large spike in day-time temperature on the 5th of April which may have further intensified the level of stress experienced by photosymbiotic organisms at this location (Fig. 2). While a higher level of cloud cover is often hypothesized to explain differential spatial bleaching patterns, we find no evidence to suggest the Bonaparte Archipelago was cloudier than the other regions where bleaching was reported (Fig. S2, Table S4). Moreover, the level of cloud cover at all surveyed locations of interest was highly variable (see overlapping error bars on Fig. S2). Additionally, the Bonaparte Archipelago was not directly impacted by any severe cyclone prior to the 2012 survey, and hence, there is no reason to consider the 2012 dataset represents a ‘low-point’ in the level of coral cover recorded.

Consistent with the previous historic records (see Jones et al. 2017), our surveys documented a remarkably diverse benthic community. Across 13 survey sites, 373 benthic species from eight classes, 28 orders and 95 families were recorded on belt transects. Scleractinian corals were abundant, with 205 species of scleractinian corals from 44 genera, seven of which were new records for the Bonaparte Archipelago (Tables S5, S6). Five suborders of the Alcyonacea were present, representing 12 families, 29 genera and 45 species of which, at least 24 of which are photosymbiotic (Table S7). A total of 52 sponge species were recorded, three of which were new records for the Bonaparte Archipelago and two of which are photosymbiotic (Table S8). A total of 71 marine mollusc species from 43 families were recorded (Table S9), including a photosymbiotic nudibranch, Pteraeolidia semperi (Facelinidae) (Fig. 2c) and two species of photosymbiotic giant clams (Fig. 2d, e). For further details and discussion about the way benthic cover varied across survey sites and between intertidal and subtidal zones, see Table S10; and for further details about incidental observations of Acanthaster planci, see Figure S5.

This study substantiates that the Bonaparte Archipelago provided a regional refuge for a diverse assemblage of photosymbiotic benthic fauna during the 2016 anomalous El Niño-associated thermal stress event. In addition to the physical mechanisms that may have driven spatial variation in bleaching susceptibility, numerous other hypotheses have previously been proposed to explain the apparent thermal resistance of the Bonaparte Archipelago coral communities (Richards et al. 2015). One of these relates to the presence of as-yet-unresolved physiological or genomic adaptations of the holobiont. It is likely that the physically demanding conditions in the Kimberley impose strong selective pressures, and less-tolerant genotypes may have been historically purged from the population resulting in a contemporary community of locally adapted photosymbiotic benthic fauna with elevated thermal tolerance thresholds, although this remains to be empirically tested. Schoepf et al. (2015) used thermal stress experiments to show that individuals from intertidal reef habitats with highly fluctuating temperatures have enhanced thermal tolerance and recovery potential in comparison with subtidal corals, and this finding is consistent with the work in other thermally variable reef environments (e.g., Oliver and Palumbi 2011; Castillo et al. 2012).

Organisms that have been historically exposed to dynamic environmental conditions are increasingly interpreted as being less vulnerable to climate change (Castillo et al. 2012). This study demonstrates that during the 2016 thermal stress event, the Bonaparte Archipelago played a role as a regional refuge, but in this instance, physical parameters are likely to have strongly mediated bleaching susceptibility; hence, the capacity for this location to act as refugia under future climate scenarios requires further investigation. Given only a limited number of ecological refuges have been identified to date including the Red Sea (Fine et al. 2013; Osman et al. 2018) and Dongsha Atoll (Tkachenko and Soong 2017), further research is warranted to substantiate the physical and biological mechanisms that may underpin the observed resistance of the Bonaparte community to current levels of thermal stress. Nevertheless, contrary to the situation in the Red Sea where eutrophication threatens to compromise the resilience of corals (Wiedenman et al. 2012; Hall et al. 2018), the lack of anthropogenic influences on the coral reefs in the Bonaparte Archipelago further enhances the likelihood that this region can persist as an internationally significant refuge for photosymbiotic organisms that are threatened by cumulative impacts in other parts of their distribution range.



The project was undertaken as a subproject of WAMSI 1.1.1 with support of Patrick Seares, Stuart Field and Andrew Heyward. It was funded by the Western Australian Museum, Woodside Energy, the Net Conservation Benefits Fund and ARC Linkage Project LP160101508. We are grateful to Tom Vigilante from the Wunambal Gaambera Aboriginal Corporation for research facilitation and Wunambal Gaambera Rangers Leonie Cheinmora and Marlene Djanghara for participating in fieldwork.

Authors’ contributions

ZR conceived the project. ZR and NW co-led the field expedition, obtained traditional owner permissions and acquired funding. RG conducted all environmental analyses. GM, JF, LK, MB, CB participated in fieldwork. AH created the map. All WA Museum affiliated authors contributed to species identifications and edited the draft. ZR, RG, GM and NW wrote the manuscript.

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Supplementary material

338_2019_1809_MOESM1_ESM.docx (19.3 mb)
Supplementary material 1 (DOCX 19776 kb)


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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Zoe T. Richards
    • 1
    • 2
    Email author
  • Rodrigo Garcia
    • 2
    • 3
  • Glenn Moore
    • 1
  • Jane Fromont
    • 1
  • Lisa Kirkendale
    • 1
  • Monika Bryce
    • 1
  • Clay Bryce
    • 1
  • Ana Hara
    • 1
  • Jenelle Ritchie
    • 1
  • Oliver Gomez
    • 1
  • Corey Whisson
    • 1
  • Mark Allen
    • 1
  • Nerida G. Wilson
    • 4
    • 5
  1. 1.Department of Aquatic ZoologyWestern Australian MuseumWelshpool DCAustralia
  2. 2.School of Molecular and Life SciencesCurtin UniversityBentleyAustralia
  3. 3.School for the EnvironmentUniversity of Massachusetts BostonBostonUSA
  4. 4.Molecular Systematics UnitWestern Australian MuseumWelshpool DCAustralia
  5. 5.School of Biological SciencesUniversity of Western AustraliaCrawleyAustralia

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