Uneven declines between corals and cryptobenthic fish symbionts from multiple disturbances

Host and mutual symbionts decline at different rates following consecutive cyclones and bleaching

Before and after disturbances, we surveyed Acropora corals known to host Gobiodon coral gobies along line (30 m) and cross (two 4-m by 1-m belt) transects. In February 2014, prior to cyclones and bleaching events, most of these Acropora corals were inhabited by Gobiodon coral gobies. Gobies were not found in corals under 7-cm average diameter, therefore we only sampled bigger corals. The vast majority of transects (95%) had Acropora corals. On average there were 3.24 ± 0.25 (mean ± standard error) Acropora coral species per transect (Fig. 2a) and a total of 17 species were observed among all 2014 transects. Average coral diameter was 25.4 ± 1.0 cm (Fig. 2b), with some corals reaching over 100 cm. Only 4.1 ± 1.4% of corals lacked any goby inhabitants (Fig. 2c). On average there were 3.37 ± 0.26 species of gobies per transect (Fig. 2d) and a total of 13 species among all 2014 transects. In each occupied coral there were 2.20 ± 0.14 gobies (Fig. 2e), with a maximum of 11 individuals of the same species.

In January–February 2015, 9 months after Cyclone Ita (category 4) struck from the north (Supplementary Fig. 1), follow-up surveys revealed no changes to coral richness (p = 0.986, see Supplementary Table 1 for all statistical outputs) relative to February 2014, but corals were 19% smaller (p < 0.001, Fig. 2a,b). Cyclonic activity may have damaged existing corals³¹, which might explain smaller corals. Alternatively, corals may have died from cyclonic damage³¹, but previously undetected corals (less than 7-cm average diameter threshold for surveys) may have grown and accounted for finding smaller corals and no changes to species richness. After the cyclone, gobies occupied 76% of live corals, which meant that occupancy dropped by 19% (p < 0.001, Fig. 2c). Goby richness did not change after the first cyclone relative to February 2014 (p = 0.997, Fig. 2d). However, goby group sizes (i.e., the number of gobies within each coral) were 28% smaller (p < 0.001), with gobies mostly occurring in pairs, and less so in groups (Fig. 2e). Smaller groups were likely due to their coral hosts being smaller than before the cyclones as there is an indirect link between group size and coral size³².

In January–February 2016, 10 months after Cyclone Nathan (category 4) struck from the south (Supplementary Fig. 1), our follow-up surveys revealed 26% fewer coral species (p = 0.008), and 13% smaller corals (p = 0.029) relative to February 2015 (Fig. 2a,b). Many corals were damaged (personal observations), and bigger corals were likely heavily damaged and disproportionately reduced in size. As Acropora corals vary in several morphological traits such as branch thickness, such characteristics might alter their susceptibility to cyclonic damage^31,34 and likely explain a decrease in coral richness. There was no change to coral occupancy by gobies relative to February 2015 (p = 0.167, Fig. 2c). Goby richness however did not mirror declines to their coral hosts as there was no change relative to February 2015 (p = 0.060, Fig. 2d). Goby group size did not change relative to February 2015 and most individuals occurred only in pairs (p = 1.000, Fig. 2e). Since the second cyclone did not add additional changes to coral occupancy, goby richness or goby group size, gobies may have exhibited some ecological memory³⁰ from the first cyclone. However, when combining the effects of consecutive cyclones, coral and goby symbioses were disrupted substantially. Coral hosts were 30% smaller relative to 2014 (pre-disturbances), 25% of hosts were uninhabited compared to only 4% in 2014, and goby group size remained the same as after the first cyclone whereby gobies were no longer living in groups, instead living in pairs (Fig. 1b). These acute disturbances had effects lasting longer than 10 months and will likely require many years to return to pre-disturbance status¹⁴.

Unfortunately, there was no time for recovery from cyclones before two prolonged heatwaves caused widespread bleaching in March–April 2016 and February–May 2017 (Supplementary Fig. 1). Ten months after the second bleaching event (Jan–Feb 2018), we returned to Lizard Island and rarely found live corals along our transects. Half (50%) of the transects lacked any living Acropora corals compared to just 5% of transects before any disturbance (2014). There were 39% fewer coral species (p = 0.009) relative to February 2016, with only 1.5 ± 0.31 species per transect (Fig. 2a). Corals were 47% smaller than in February 2016 (p < 0.001, Figs. 1b, 2b), averaging 9.57 ± 0.39 cm coral diameter (maximum 21 cm). Acroporids were also the most susceptible family to bleaching from these back-to-back heatwaves across the Great Barrier Reef and their coral recruitment was at an all-time low^2,16. Since corals were lethally bleached during the prolonged heat stress, only a few acroporids species survived these consecutive events³⁵. Such declines and extensive bleaching from the 2015–2016 heatwave were also observed in many areas around the world^5,36.

After consecutive heatwaves, coral gobies faced even more drastic declines than their coral hosts in all our survey variables. Of the few live corals recorded, most (77.7 ± 4.8%) corals lacked gobies compared to just 4% without gobies pre-disturbance (2014), and 24% after cyclones (p < 0.001, Fig. 2c). For the first time, only after heatwaves, we observed a change in goby richness with 80% fewer goby species per transects relative to February 2016 (p < 0.001, Fig. 2d), even though consecutive cyclones did not affect goby richness. Alarmingly, goby group size decreased to such an extent that gobies were no longer found in groups (p = 0.036), rarely in pairs (n = 3), and the few observed occurred singly (Fig. 2e). For these long-living, monogamous, and nest brooding fishes^28,37, finding gobies predominantly without mates suggests that reproduction likely ceased or was significantly delayed for most individuals in the population²⁸. An interruption in mate pairing likely led to extremely low recruitment and turnover rates in gobies from climatic disturbances.

Gobies declined substantially more than coral hosts after consecutive heatwaves, leaving most corals uninhabited (Fig. 1b). Although communities still had not recovered from cyclonic disturbances before prolonged heatwaves, we suspect that heatwaves had more devastating impacts on gobies than cyclones. Gobies have a strong tendency to stay in the same coral they settle in as recruits³⁸ as long as the coral is alive³⁹, yet many may have unsuccessfully attempted to find other corals once their coral was lethally bleached⁴. Unlike gobies, other coral-dwelling fishes, like damselfish recruits, successfully adopted alternative habitat, including dead corals⁴⁰. Gobies did not adopt alternative habitat and were surprisingly absent from most living corals.

Importantly, goby richness did not change after consecutive cyclones and only changed after heatwaves. Thus coral host death likely is not the only stressor and gobies may have suffered physiological consequences from prolonged environmental disturbances^41,42,43. Although gobies can survive short exposures of hypoxia⁴⁴, extended periods of reduced wind-induced mixing and thermal stress may jeopardize physiological functioning^45,46. Indeed, reef fishes can lose the ability to detect predators, kin, and habitat^41,42,43, and to reproduce from environmental stress⁴⁶. Gobies likely lost similar functioning from heatwaves leading to high mortality and little goby turnover, which left many healthy corals unoccupied. A lack of mutual goby symbionts following consecutive disturbances suggests that coral hosts may begin experiencing additional threats to their recovery^19,20,21. Such declines and potential physiological consequences may also hold true for other coral-dwelling organisms, like symbiotic xanthid crabs⁴⁷. Since acroporid corals are crucial foundation species for coral reef ecosystems, greater declines in their symbionts from multiple disturbances may reduce the persistence of corals and destabilize habitats over large scales.

Communities of goby symbionts exhibit greater changes than communities of coral hosts from multiple disturbances

In February 2014, before the consecutive climatic events, we recorded 17 species of Acropora corals known to host Gobiodon coral gobies, with the most common being A. gemmifera, A. valida, A. millepora, A. loripes, A. nasuta, A. intermedia, A. tenuis, and A. cerealis. Thirteen species of Gobiodon gobies were recorded, with the most common being G. rivulatus, G. fuscoruber, G. brochus, G. histrio, G. quinquestrigatus, and G. erythrospilus. Each disturbance changed the assemblages of both corals (p < 0.001, Fig. 3a) and gobies (p < 0.001, Fig. 3b), yet the changes in both corals and gobies did not mirror each other since communities among sampling events did not aggregate similarly (Fig. 3).

After the first cyclone, 11 Acropora species were found, and the common species increased in proportional abundance relative to February 2014 (p = 0.009, Figs. 3a, 4a). The previously rare species A. valida increased in proportional abundance as well. However, Acropora intermedia, which was previously recorded in several transects, was no longer observed; this is likely due to its branches being long and thin, thus highly susceptibility to damage³¹. Goby assemblages were also altered after the first cyclone (p = 0.003, Fig. 3b), and the proportional abundance of the common species differed in response relative to 2014 (Fig. 4b). The proportion of G. histrio and G. rivulatus in transects increased compared to 2014, and so did the proportion of their preferred hosts, A. nasuta and A. gemmifera, respectively (Fig. 4)⁴⁸. However, the proportion of G. fuscoruber decreased even though its common host, A. millepora⁴⁸, was recorded more frequently than several other corals (Fig. 4). Gobiodon fuscoruber is a group-living species, and it is possible that as group size decreased, they were outcompeted for coral hosts by other species⁴⁹. Two rare gobies were no longer recorded (G. citrinus and G. okinawae), and both preferred A. intermedia⁴⁸, which also disappeared. Since species of both corals and gobies had mixed responses to the cyclone, there may be some positive effects of an intermediate level of disturbance for those species that increased in proportional abundance, specific to the intermediate disturbance hypothesis⁵⁰.

After the second cyclone, we found mixed results in coral assemblages (p < 0.001, Fig. 3a). Although 15 Acropora species were found after the second cyclone (5 more than after the previous cyclone) and no species were locally extirpated, only A. loripes became more common (Fig. 4a). Several of the most common corals (i.e. A. gemmifera, A. nasuta, A. tenuis) decreased in proportional abundance after the second cyclone (Fig. 4a). Goby communities were altered once again (p < 0.001, Fig. 3b), this time with fewer species increasing in proportional abundance and more species decreasing (Fig. 4b). However, all Gobiodon species were encountered, even G. citrinus and G. okinawae that originally disappeared after the first cyclone. Gobiodon brochus increased in proportional abundance and so did its common host A. loripes⁴⁸. However, G. rivulatus increased even though its preferred host A. gemmifera decreased (Fig. 4)⁴⁸.

After consecutive bleaching events, the reef was left with few corals, most of which were very small in size. Although the coral community after bleaching was distinct from each disturbance sampling event (p < 0.001), all disturbed communities aggregated closely together compared to the pre-disturbance community (2014, Fig. 3a). After bleaching, the most coral species were recorded (22 in total) compared to all other sampling events. Although coral richness per transect was the lowest after bleaching (Fig. 2a), the coral community as a whole was more diverse and was made up of more coral species. A few A. intermedia were again recorded after none were observed following the first cyclone, along with 9 rare and previously unrecorded Acropora species. However, some species were no longer observed, e.g. A. divaricata (previously rare), A. granulosa (previously rare), and A. humilis (previously common). Many of the common coral species became rare after bleaching (Fig. 4a). In coral reefs, Acropora are one of the most susceptible coral genera to cyclone damage and bleaching in a warming climate^16,31, which explains such steep declines in many Acropora species. Surprisingly, A. cerealis, which was previously rare, had since increased in proportional abundance despite multiple disturbances (Fig. 4a). In other areas though, such as the Andaman Bay, A. cerealis was one of the most lethally bleached species³⁶. Regional differences in thermal plasticity and coral recruitment may have disproportionately affected the survival thresholds of identical species.

Coral gobies were more dramatically affected by consecutive bleaching than corals. Goby communities after bleaching were the most distinct (p < 0.001), while communities from all other sampling events aggregated closer together (Fig. 3b). Every goby species declined after bleaching (Fig. 4b), and half of the species were no longer recorded. Some species were locally extirpated, including G. citrinus (previously rare), G. sp. D (previously rare), G. bilineatus (previously common), and G. fuscoruber (previously common, Fig. 4b). None of the locally extirpated species were observed during random searches. Only 6 species remained, and no previously unrecorded species were observed. As expected, gobies were never found in dead corals, as they can only survive in live corals (albeit surviving in stressed corals³⁹). These findings highlight the greater impact that multiple disturbances have on symbiont communities, especially when disturbances are a mix of acute (short-term) and prolonged (long-term) events. Although we cannot assess the effects of cyclones compared to heatwaves since they occurred in succession, we can clearly show that multiple disturbances affect corals and gobies differently. We observed a loss of biodiversity for gobies from multiple disturbances, whereas their coral hosts were more diverse even though fewer corals were recorded and they were smaller.

The study demonstrates the effects that multiple disturbances have on reef ecosystems down to the level of important mutualisms. Disturbance studies have primarily focused on the disturbance effects to corals^16,30,31, yet cryptobenthic fishes are often overlooked⁴. We may be missing effects of disturbances on fishes that could have flow-on effects on the whole ecosystem, especially since cryptic fishes make up a large portion of reef biodiversity and are crucial prey for many taxa⁴. This study is one of few multi-year studies to record species-level changes in cryptobenthic fishes from multiple consecutive disturbances. Intriguingly, although corals and gobies responded similarly at first to the initial two cyclones, they then diverged in their responses after additional stress from heatwaves. Here we show that gobies declined faster on a community and species level than their coral hosts, which will likely leave corals exposed to algal growth, poor nutrient cycling, and corallivory^19,20,21 (Fig. 1). The unwillingness of gobies to use alternative habitat in the short-term may drastically reduce their resilience to disturbances, threatening localized extinction⁵¹. Declines from a single disturbance have the potential for a resilience, but multiple events will require long-term recovery^31,32 as most corals are uninhabited after consecutive disturbances (Fig. 1b). Although the disturbances in this study were compounded, heatwaves may have had an even stronger effect on gobies since goby communities differed the most after the heatwaves, whereas coral communities remained similarly diverse after each disturbance. Without the added benefits of gobies, surviving corals will likely experience further threats to survival^19,20,21. Multiple disturbances may even cause ecosystem shifts when the foundation species of the environment, such as hard corals, face extreme declines⁶. If mutual symbionts show greater declines than corals as seen in this study, important processes may be exacerbated, further jeopardizing the recovery potential of an ecosystem’s foundation species.

Future implications for symbiotic relationships from multiple disturbances

Our study demonstrates that consecutive disturbances result in uneven declines between mutual symbionts, and this has the potential for exposing surviving hosts to additional threats if their mutual and cryptic inhabitants disappear. As mutualisms break down, organisms that rely on these mutualisms may become more vulnerable to multiple disturbances and there may be ecosystem-level disruptions as a result^1,6,13,24, especially as climate-driven events becomes more frequent⁵. Although the length and type of the disturbance play important roles in disturbance impacts, few studies have examined the effect of multiple disturbances^30,31,52. If successive threats become the norm, a system will already be stressed before a second event strikes, leading to greater consequences³¹. Population bottlenecks will inevitably follow³ and threaten the survival of many organisms globally⁷. Flow-on effects will affect closely-associated organisms, especially for those that depend on feedback loops with symbionts⁶. In each ecosystem, species are responding differently to disturbances, and mutually beneficial relationships are being tested⁶. Our study suggests that multiple disturbances will likely leave ecosystem builders exposed to additional threats if their cryptic symbionts fail to recover.

Source: Ecology - nature.com