Environmental generalism, holobiont interactions, and Pocilloporid corals in the warming oceans of the eastern coast of Australia
Jessica L. Bergman
Zoe T. Richards2,3 
Tracy D. Ainsworth- 1Biological, Earth, and Environmental Sciences, University of New South Wales, Sydney, NSW, Australia
- 2Coral Conservation and Research Group, Trace and Environmental DNA Laboratory, School of Molecular and Life Sciences, Curtin University, Bentley, WA, Australia
- 3Collections and Research, Western Australian Museum, Welshpool, WA, Australia
- 4School of Environmental and Life Sciences, University of Newcastle, Callaghan, NSW, Australia
Ocean warming has been driving mortality events across the world’s coral reef ecosystems and is resulting in multifaceted ecosystem restructuring. With the rapid shifts occurring across ecosystems, questions arise of which species, in which locations, have the capacity to persevere under climate change. Environmental generalism refers to species with the biological traits that support environmental flexibility, enabling the organism to occupy a broad range of environmental conditions. Some Scleractinia have been categorised as environmental generalists and proposed as likely winners under changing climate conditions, as environmental generalists have been considered less susceptible to environmental disturbance than specialist species. Given the complexity of the holobiont structure of corals, which includes photoendosymbiosis and diverse microbial consortia, understanding the complexity of the coral holobiont–environment interaction for the generalist corals will be an important factor in accurately predicting the success of these species into the future. Here we conduct a literature search to compile topics and concepts of environmental generalism for Australia’s warming coral reef ecosystems and the breadth of holobiont responses to ecosystem restructuring. We synthesise these findings in the context of the latitudinal expanse of Australia’s coral reefs to highlight how it is necessary to understand the biological underpinnings of generalist corals.
1 Introduction
Scleractinian, or hard (stony) corals are most widely known for their role as the trophic and structural foundation of coral reefs, particularly for reefs in warm, shallow, tropical waters (Hamylton et al., 2022). While corals dominate tropical reefs and provide the foundation for the most diverse ecosystems on the planet, corals are also found across a breadth of light and temperature regimes outside of reef forming structures, including within sandy bays, caves, coastal waterways, mangroves, seagrass beds, temperate waters and the deep sea (Perry and Larcombe, 2003; Cairns, 2007; Richards et al., 2016; Camp et al., 2019; Watanabe and Nakamura, 2019; Burt et al., 2020). In addition to being found across a range of marine ecosystems, this highly diverse group of organisms exhibits a wide variety of life history traits, growth forms, and adaptations to the array of environmental regimes in which they are found (Jackson, 1991; Connell et al., 2004; Todd, 2008; Zawada et al., 2019; Bairos-Novak et al., 2021). This diversity of coral life highlights the challenges that arise when forecasting the role this taxa will play in ecosystem restructuring under environmental change.
Global coral reef ecosystems, dominated by reef-forming scleractinia (Pandolfi et al., 2011; Vermeij et al., 2011; Hughes et al., 2018; Cornwall et al., 2021; Eddy et al., 2021), are undergoing significant changes due to anthropogenic climate change. Record warm temperatures and rates of warming are disrupting coral photoendosymbiosis and causing widespread whole organism heat-induced and bleaching-induced mortality across the world’s coral reefs (Donovan et al., 2021; Hughes et al., 2021). As bleaching events increase in frequency, the impact of these disturbance events accumulates and affects the capacity of the ecosystem to recover (Dietzel et al., 2021). In one well-documented study undertaken between 1968 and 2004, comprising 6001 benthic surveys of 2,667 Indo-Pacific reefs, a 1–2% yearly decline in coral cover was demonstrated (Bruno and Selig, 2007). Similarly, in the Seychelles, a 17-year data set demonstrated mass bleaching events reduced live coral cover by > 90% in the reefs surveyed, leading to a shift towards a macroalgae-dominated ecosystem in nine out of 21 reefs (Graham et al., 2006; Graham et al., 2015). A time-series analysis of coral reefs in Moorea, French Polynesia found extensive coral loss and change in abundance of the major coral genera on the reef between 1979 and 2009 due to the cumulative impacts of Acanthaster planci outbreaks, cyclones, and bleaching (Pratchett et al., 2011). A similar trajectory has been reported for coral reefs in Okinawa, Japan, where net coral area declined 42–72% and changes in abundance of the dominant scleractinian taxa followed bleaching events, typhoons, and increased sedimentation (Harii et al., 2014). The recent coral cover report for the Great Barrier Reef by the Australian Institute of Marine Science (AIMS, 2022) also suggested that short-term gains in coral cover following severe bleaching and mortality events in 2021/2022 highlighted long-term impacts of shifting population structure to fast growing but thermally susceptible coral species. Fast-growing Acropora species, which drive recovery on damaged reefs, are also the most vulnerable to the common disturbances affecting the GBR (AIMS, 2022). These examples underscore widespread coral reef degradation from biological and anthropogenic stressors (Eddy et al., 2021). As such, coral reefs are now being altered in historically unprecedented ways (van Woesik et al., 2012).
The vast ecosystem restructure occurring in marine ecosystems has also been shown to include the replacement of historically dominant coral species with corals exhibiting more persistent, weedy, and opportunistic traits (Knowlton, 2001; McClanahan et al., 2007; de Bakker et al., 2016; Caballero Aragón et al., 2019; McWilliam et al., 2020; Cornwall et al., 2022). Generalist coral species, or those that thrive across a breadth of environmental conditions and are considered more tolerant of sub-optimal conditions than species within a narrow environmental niche (Richmond et al., 2005; Clavel et al., 2011; Darling et al., 2012), are hypothesised to play an important role in this population restructure (Courtney et al., 2020). In contrast, specialist species may be more susceptible to metapopulation dynamics under climate change, with potential extinction risks due to decreased effective population size and genetic variation in already small populations; this has been seen in butterflyfish (Lawton et al., 2011), marine teleosts (Smith and Fujio, 1982), and marine molluscs (Lavm and Nevo, 1981). Generalist coral species may be more successful than specialist coral species on reef ecosystems as the climate continues to change (Clavel et al., 2011; Chichorro et al., 2019), offering critical ecological opportunities for the reconfiguration of coral reefs. As such, addressing knowledge gaps in the potential for these species to expand into new habitats as ecosystem restructuring occurs is crucial for predicting both future reef structure and coral extinction risk (Bridge et al., 2020).
1.1 Terminology used in environmental generalism research for corals and coral reef ecosystems
Generalist species have been defined in ecology as those that exploit multiple habitat types or food sources, while a specialist is limited to only one or a few (van Tienderen, 1991). There are several ecological predictions that have been linked to both generalist and specialist species that hypothesise various uses of resources determine the range size of the species (Slatyer et al., 2013).This hypothesis states generalist species are more likely to have a higher tolerance towards habitat loss and climate change due to their adaptabilities and large range sizes through positive correlations between niche breadth and geographic range. Generalist species with a broad resource breadth are thought to be more persistent because they are less sensitive to stochastic fluctuations of any given resource. This concept is also the foundation of the generalism–specialism debate, where generalism in resource use and niche breadth has been suggested to create an ongoing cycle where the success of generalists drive speciation and species extinction (Dennis et al., 2011). However, there is clearly a wide range in how generalist species and their role in their environment is defined.
The terms “generalist species”, “generalism” and “generalist coral” appear to be underutilized and inconsistently applied in coral reef research. For example, a search of primary research publications for the terms <generalist AND coral> between 2010 and 2022 identified 187 articles, of which only 72 studies related to specifically to Scleractinian coral species (opposed to other species within coral reef ecosystems). Of these studies, 2 species, Montastrea cavernosa and Stylophora pistillata, were the primary study species in the research conducted (Table 1). While definitions for generalist species and use of generalist terminology has varied in the primary literature, the research that has used these terms to-date has classified generalist species by the taxa within-reef distribution, with 68% of studies identified here referring to depth generalists (Figure 1). Generalist corals have also been defined through:
1) flexibility of their relationship with Symbiodiniaceae and the bacterial microbiome (16% of the identified studies),
2) variation in life history traits (11% of identified studies),
3) a broad environmental distribution (4% of identified studies), and
4) plastic morphology (1% of identified studies).
Table 1 72 publications returned in a Google Scholar search for the terms <generalist AND coral> between 2010 and 2022, sorted into five primary categories used to define generalists in the literature: depth, environmental, life history, morphology, and symbiont.
Figure 1 (A) Percentage of the 72 studies included in the present manuscript that are focused around each category of generalism. (B) Number of studies per taxa considered “generalists” in the 72 studies considered herein. “Various or Review” refers to studies that didn’t specify taxa or that contained mention of the terms <generalist AND coral> in a review, respectively.
Two studies have conducted the most extensive categorisation of coral species within generalist and specialists groups:
Firstly, Darling et al. (2012) applied a trait-based classification approach for 143 species of coral, defining generalist species as those having life history traits of competitive, weedy, and stress-tolerant corals. Competitive species have traits that align with specialist species, such as efficiency in using resources and dominance in highly populated, ideal environments. Weedy corals have fast reproduction times and diverse species traits, which allows them to opportunistically colonise a variety of disturbed environments. Stress-tolerant corals are defined as those with slow growth, long generation times, large corallites, and high fecundity that help them to proliferate in chronically harsh environments. Generalist corals have overlapping traits with both weedy and stress tolerant corals, as defined by Darling et al. (2012), and we refer to corals with this set of traits as “generalists” from here on out. Sommer et al. (2014) also utilised trait-based filtering for corals along a latitudinal gradient in high-latitude eastern Australia, finding high-latitude coastal reefs to be mainly dominated by generalist coral species of massive morphologies, which persist in conditions of high environmental stress but also contribute to a low structural complexity and have limited recovery potential following disturbance due to slow-growing trait of massive morphotypes. However, consistent with Darling et al. (2012), the authors also found that species with similar functional characteristics have higher co-occurrence. This raises the question of how abiotic filtering (e.g. environmental parameters) will influence the structure of coral communities when corals with different life-history strategies (e.g. different growth rates or reproductive modes) share similar traits.
Table 2 summarises trait-based classifications used in the studies of Darling et al. (2012), Darling et al. (2019) and Sommer et al. (2014) to further elaborate on how generalist species can encompass a combination of various life history strategies or be composed of a subset of competitive taxa (as defined by Darling et al., 2012). The ambiguity in defining generalist species highlights a knowledge gap crucial for predicting and managing the form and function of future reefs and optimising conservation planning. Pocilloporid corals (Gray, 1840) are a widespread taxonomic group of scleractinian corals that have been reported on coral reef ecosystems worldwide across vast geographic, environmental, and depth ranges (Figure 2). Known to be a fast-growing and opportunistic genus (Brustolin et al., 2019), Pocilloporids serve as an example of generalist traits due to both high levels of phenotypic plasticity and a broad environmental distribution (Todd, 2008; Schmidt-Roach et al., 2014; Putnam et al., 2020; Burgess et al., 2021). The capacity for plasticity in the group contributes to the challenge of identifying species, species complexes and species ranges in addition to having substantial genetic variability amongst visually similar species (Todd, 2008). For example, Pocillopora damicornis has traditionally been described as four distinct ecomorphs – elongate, semi-disturbed, compact, and branching (Veron and Pichon, 1976). Recent studies have therefore used genetic and morphometric evidence to differentiate species within the Pocilloporids, with Schmidt-Roach et al. (2014) describing eight species within the P. damicornis species complex (including a novel taxon Pocillopora bairdi). Johnston et al. (2022) genetically identified 673 colonies in the Pocillopora species complex around Mo’orea, French Polynesia, and found that the 4 most abundant species were often visually indistinguishable yet exhibited clear physiological differences in response to light and water temperature variance. These studies indicate that while many Pocilloporid species are visually indistinguishable, genetic differences may be associated with distinct traits that affect their success in a changing environment. The misinterpretation of taxonomical units within species, e.g. for Pocillopora damicornis (Schmidt-Roach et al., 2012), contributes to challenges of disentangling morphological and life history variation with environment. This further highlights the complexity and plasticity of the Pocilloporid family. The wide variety of responses recorded between coral host, algal symbionts, bacterial microbiome (“holobiont”), and the holobiont–environment interaction, suggests that generalist corals such as the Pocilloporidae may have the breadth of plastic traits necessary to survive in a changing world. Here we review (1) the traits of the Pocilloporid holobiont associated with environmental generalism; (2) the aspects of holobiont–environment interaction that would support the assumption of environmental generalism in this genera; and (3) the intersection of environmental generalism, holobiont structure, and the restructuring of a diverse range of coral habitats across Australia’s east coast.
Table 2 A summary of trait-based classifications used by Darling et al. (2012), Darling et al. (2019), and Sommer et al. (2014) to define generalist species and three life-history forms contained within: weedy, stress-tolerant, and competitive.
Figure 2 A schematic illustrating the five domains of generalist species defined in the literature search conducted herein, and how traits common to Pocilloporids apply to each domain. Black text arrows indicate how Pocilloporids may respond to influence their success when environmental pressures (e.g. increased light, rising temperatures, physical forcing) are applied.
2 Generalist traits and the Pocilloporid holobiont
2.1 Morphological plasticity
Pocilloporid corals have a high degree of plasticity in overall skeletal morphology across environments (Todd, 2008; Johnston et al., 2017). Pocilloporids increase in compactness with increasing water motion (Kaandorp, 1999), vary in branch structure concurrent with degree of reef exposure (Lesser et al., 1994), and can appear elongate in subtropical regions while being robust in tropical regions (Schmidt-Roach et al., 2014). Furthermore, water flow and wave motion were found to systematically ordinate Pocillopora colony structure in Mo’orea, French Polynesia (Corso et al., 2022), due to physical forcing that likely aligns colonies with the dominant direction of the wave energy. Pocilloporids can also exhibit microstructural plasticity in response to light, water movement, and depth. Pocilloporid microstructure is influenced by environmental parameters, for example significant variation in 17 micro- and two macrostructural characteristics was observed in Pocillopora verrucosa colonies found between 7 and 38–45m depth (Gélin et al., 2018).
2.2 Tissue structure and within-colony symbiont distribution
Biological traits of tissue structure and its influence on symbiont distribution within a colony are believed to support vast environmental tolerance, including depth and light tolerance. In a study by Terraneo et al., examining symbiont types in shallow and mesophotic corals in the Red Sea, Durusdinium spp., known to assist with stress and thermal tolerance, was found predominately in shallow water corals compared to mesophotic corals (Terraneo et al., 2023). This suggests that symbiont distribution may be host and environment specific. Pocilloporids, characterised by an imperforate tissue structure that lacks intercalating tissues in a skeletal matrix (Yost et al., 2013), exhibit adaptability to diverse environmental conditions due to their shallow tissue depth. This tissue structure that predominantly extends across the surface of the skeleton contrasts with the tissue structure within the matrix of the colonial skeleton that is seen in perforate corals. Another potential contributing factor to the flexibility of Pocilloporids across different depths is their highly variable symbiont distribution related to light penetration and amplification within the colonies (Terán et al., 2010). Interestingly, Pocilloporids are the only genera that have been linked to polyp bail out responses (Fordyce et al., 2017; Chuang and Mitarai, 2020; Gösser et al., 2021), wherein individual polyps disassociate from a colony under stress and re-settle on the benthic substrate. It is important to note that to date the role of polyp bailout responses in Pocilloporid recovery of coral cover (Fordyce et al., 2017) following severe bleaching events has not been well investigated.
2.3 Bacterial microbiome stability
Several thousand microbes have been discovered within the coral microbiome (Rohwer et al., 2002). These are comprised of archaea, bacteria, viruses and Symbiodiniaceae (Symbiodinium) which inhabit the coral tissues, skeleton, mucus and gastrovascular cavity (Osman et al., 2018). These microbial interactions can either be mutualistic, parasitic or symbiotic interactions (Aranda et al., 2016). The ubiquitous distribution of Pocilloporid corals across environments have made them a well-studied target in coral bacterial microbiome research since 2018, characterising the Pocillopora microbiome across the Indo-Pacific and Red Sea. There also evidence that the coral microbial associations with P. damicornis may be a factor influencing bleaching response in these corals (Gilbert et al., 2012); namely, widely observed microbial patterns in response to bleaching may contribute to Pocillopora’s classification as a generalist. These include microbial stability during bleaching and across different environmental conditions (Ziegler et al., 2019; Brener-Raffalli et al., 2018; Pogoreutz et al., 2018; Epstein et al., 2019; Maher et al., 2020; Bergman et al., 2021). Some studies have found that despite severe bleaching in P. damicornis (e.g. loss of symbionts, but no mortality), bacterial communities did not increase in diversity, change, or become pathogen dominated; rather, the community structure resembled that of healthy P. damicornis colonies (Bergman et al., 2021). Similar findings have been observed in P. damicornis larvae, where Symbiodinium cell densities of larvae decreased under high temperature conditions, but no reduced survivorship was observed (Haryanti et al., 2015). Bacterial shifts in response to bleaching have been observed, for example shifts in Symbiodinium-associated partner bacteria, such as Lactococcus and Bacillus, in Pocillopora verrucosa colonies during a natural bleaching event in the South China Sea (Yang et al., 2021). Interestingly, in a study of P. acuta, the microbiome was found to respond rapidly and flexibly to transplantation in Singapore, becoming similar to that of the local colonies at the transplanted reef within 1–2 days of transplantation (Deignan and McDougald, 2022). Even in stable communities, Endozoicomonas is a bacterial associate consistently found in the microbiome of Pocilloporid corals (Pogoreutz et al., 2018; Epstein et al., 2019; Voolstra and Ziegler, 2020; Ricci et al., 2022), with Maher et al. (2019) reporting Endozoicomonas dominate Pocillopora microbiomes that have declined in overall diversity. Microbial stability in Pocillopora in response to warming may contribute to its role as a generalist species on reefs.
2.4 Photoendosymbiont and holobiont bleaching responses
In Pocilloporid corals Symbiodinium are transferred maternally, leading to co-evolution with the host and species-specific associations of symbionts irrespective of geography (Pinzón and LaJeunesse, 2011; Schmidt-Roach et al., 2013a; Brener-Raffalli et al., 2018). Stability in patterns and composition of P. damicornis-associated Symbiodiniaceae has been found between adults and juveniles in the South China Sea irrespective of exposure to stress (i.e. ocean acidification), with a consistent dominance of the thermally tolerant endosymbiont Durusdinium spp. (Zhou et al., 2021). Endosymbiont population stability has also been observed in adult Pocillopora, with the stress-tolerant Durusdinium largely dominating the Symbiodiniaceae population in P. acuta throughout bleaching response of the host coral (Poquita-Du et al., 2020a; Poquita-Du et al., 2020b). In the Red Sea, where there are strong environmental gradients from north to south, Symbiodinium microadriaticum (type A1) has been found to dominate across a latitutinal gradient (Sawall et al., 2014). While the dominant resident Symbiodinium in Pocillopora corals often remain at a high abundance, even during stress events (e.g. cold-water bleaching, (McGinley et al., 2012), there is also some evidence of flexibility in host–symbiont combinations with variability across sites (Cunning et al., 2013) or environments (Ros et al., 2021; Botté et al., 2022). Observed interactions between physiological performance, host genotype, and symbiont communities in P. damicornis, as observed between flat or slope reef habitats of Australia’s Heron Island in Marhoefer et al. (2021), emphasise that local adaptation of colonies as a product of environmental factors is also possible and should be accounted for.
3 The generalist holobiont–environment interaction and a changing climate
The largest influences on corals is the availability of photosynthetically available radiation (PAR), which causes variations in morphology, skeletal structures, photosynthetic traits, heterotrophic feeding, and Symbiondinaceae genera (Martinez et al., 2020). Generalist species are regarded as likely to be more successful than specialists as the climate continues to change (Clavel et al., 2011; Chichorro et al., 2019) due to their ability to adjust to these influences in their environment. Understanding the holobiont traits that contribute to environmental generalism is critical to predicting the structure of reefs under future scenarios. As global climate change continues to drive ecosystem change and novel environmental conditions become increasingly prevalent, the hypothesised increased role of environmental generalists in ecosystem stabilisation is evident (Graham et al., 2014; Williams and Graham, 2019). A recent study conducted on the reefs of French Polynesia investigating a 26-year monitoring database found that corals in the genus Pocillopora now make up 84% of the total recovery rate on the reef following disturbance (Pérez-Rosales et al., 2021). While the success of some genera on disturbed reefs is beneficial for overall coral coverage, a convergence towards post-disturbance communities less diverse and dominated by a single genera, morphology or phenotype (as shown by Pérez-Rosales et al. (2021) for 5 out of the 7 reefs) is also discussed as a key risk of sudden ecosystem declines under further disturbance events (Dalin et al., 2009; Palumbi et al., 2009; Lin, 2011). Palumbi et al. (2009) emphasise the importance of preserving biodiversity on reefs, as communities dominated by a single genus are likely have a more limited range of functions in response to disturbance than reefs composed of a diverse range of genera. Dominance of a single genera, especially one that is visually indistinguishable from other species within its genera, may be due to niche differences in co-occurring cryptic species. For example, Johnston et al. (2022) found greater differential abundances of Pocilloporid species across depths than amongst sites separated by several kilometers. The four most abundant species observed in this study were visibly indistinguishable at the gross colony level, yet exhibited differences in their associations and response to light irradiance and water temperature that may further promote their proliferation across reef environments with potentially varying degrees of generalism by species (Johnston et al., 2022).
Recent monitoring on the GBR following severe bleaching events of 2016–20 have also found an increase in dominance of Pocillopora species over the previously dominant specialist Acropora species (AIMS, 2021), noting that an increase in cover of a single genera had the potential to put the reefs at greater risk in future events. Therefore, the role of environmental generalist species (those with greater plasticity for a range of some conditions) will be uncertain in highly dynamic marine environments, particularly those environments with severe and frequent extreme conditions (Munday, 2004; Camp et al., 2018).
As warming on temperate, subtropical, and tropical reefs continues to drive the emergence of novel ecosystems, efforts in conservation and ecosystem rehabilitation, repair, and restoration are now based around supporting (repair and rehabilitation) or actively undertaking (restoration) reconstruction of altered and degraded environments (Fox et al., 2019; Vardi et al., 2021; Shaver et al., 2022). Successful ecosystem repair, reconstruction or restoration involves identifying the target organisms that can acclimate and proliferate in both current and predicted future environmental conditions (Prober et al., 2015; van Oppen et al., 2017; Vardi et al., 2021; Shaver et al., 2022). Understanding the physiological range of the target organism in a dynamic environment for these types of conservation efforts will therefore be the cornerstone of the science of conservation ecology on coral reefs. Detailed understanding of the plasticity of the biological traits which underpin an organism’s success across a range of environment parameters will be key for conservation efforts, particularly those focused on organisms that show resilience and environmental plasticity (Kimball et al., 2016; Boström-Einarsson et al., 2020; Shaver et al., 2022). The broad similarities amongst Pocilloporid species in the relationship between morphology, microbiome, and plasticity across sites or environmental conditions are therefore potentially key factors contributing to the success of this genera.
4 Australia as a case study: are there locations in eastern Australia where coral reefs are resistant to environmental change?
Australia’s reefs have been subject to the impacts of climate change in recent years, and we focus specifically on several examples where reefs have been impacted by warming. We continue to build on the aforementioned point that generalist species may be better suited to acclimate to current environmental conditions (e.g. warming), but that it is critical to understand what role they will play in future reef conditions or in the highly dynamic marine environments mentioned herein. The majority of Australia’s coral reef ecosystems extend across approximately 344,400 km2 of the continent’s east coast, which includes the ecosystems of tropical coral reefs, subtropical coral reefs, and high-latitude coral reefs (Great Barrier Reef Marine Park Authority, 2012; Figure 3). Most tropical corals are found 30–200 km offshore along the shallow inshore and lagoonal reefs, submerged reefs, mesophotic and deep-water coral reefs of the Great Barrier Reef/Coral Sea (Olsson et al., 2008). Subtropical continental shelf coral populations are also found along approximately 900 km of continental shelf from the southern Great Barrier Reef to the Solitary Islands, with temperate populations now being reported as far south as Sydney Harbour (Harriott and Banks, 1995; Harriott and Smith, 2002; Linklater et al., 2016; Roelfsema et al., 2016; Linklater et al., 2018; Linklater et al., 2019). Coral populations within the subtropical-to-temperate transition zone of Eastern Australia include marine habitats with unique assemblages of corals, sea grasses, kelps and turfs (Wilson and Harrison, 2003; Vergés et al., 2016; Sommer et al., 2017; Vergés et al., 2019). Further south, merging temperate and subtropical waters supports the development of new species, unique species interactions, and distinct habitats on the world’s most southern coral reef, World Heritage-listed Lord Howe Island (Harriott et al., 1995; Noreen et al., 2009; Edgar et al., 2010).
Figure 3 A map of reef locations included along Australia’s east coast. Long dashes border the Great Barrier Reef Marine Park, dotted lines border the Coral Sea Marine Park, and dot-dash lines border the Temperate East Australian Marine Park Network. Sites are: 1). Great Barrier Reef, 2). Coral Sea, 3). Norfolk Island and Norfolk Ridge, 4). Elizabeth and Middleton Reefs, 5). Solitary Islands Marine Park, 6). The Lord Howe Seamount Chain, Lord Howe Island, and Ball’s Pyramid, and 7). Sydney Harbour. For images on the right-hand side, numbers correspond to reef location and letters depict (A) an example of a Pocilloporid from each location and (B) a whole-reef image from each location. All pictures taken by Jessica Bergman, with the exception of images reproduced with permission: 2A, 2B: Parks Australia Coral Sea Marine Park Coral Reef Health Report; 4A, 4B: Antonia Cooper; 7A, 7B: John Turnbull. Bleaching events recorded at each location are listed along the left-hand side of the photos. For 1). Great Barrier Reef: Bolded dates are years when both the N. GBR and S. GBR bleached, and dates not in bold are years when only the N. GBR bleached.
Coral reefs within Australia’s southern Great Barrier Reef and Great Southern Reef, particularly those at the convergence of sub-tropical and temperate zones, are as such experiencing climate mediated changes to species distribution and abundance, benthic habitat change, and the range extension of tropical species (Pandolfi et al., 2003; Brandl et al., 2019; Eddy et al., 2021). Warming oceans are driving high coral mortality, changes to population structure, emergence of new diseases, reduced growth, and reduced recruitment even on high-latitude reefs (generally outside of 30° N or S). Most evident of this problem is the severity and frequency of mass coral bleaching events now increasingly recorded in corals within Australia’s understudied high-latitude reefs. For example, bleaching was recorded at Lord Howe Island in 1998, 2005, 2010, 2011 and 2019, one of the highest frequencies of coral bleaching events reported in Australia (Harrison et al., 2011; Dalton et al., 2020; Steinberg et al., 2022). Additionally, mass bleaching affected 22 high-latitude coral assemblages found south of the GBR in 2016 (Kim et al., 2019). Genetic evidence shows that connectivity to larger metapopulations is limited for corals growing at the southern edge of their species range (Noreen et al., 2015; Mizerek et al., 2021), resulting in high levels of evolutionary novelty (Miller and Ayre, 2008; Noreen et al., 2009; Schmidt-Roach et al., 2013a; Noreen et al., 2015) in these locations.
The observed species composition changes observed on temperate to subtropical reefs have the potential to profoundly alter temperate marine ecosystems within the coming decades. The question arises as to whether generalist corals will be a feature of Australia’s changing east coast coral reef ecosystems as climate change continues to impact these regions. The response of generalist species, specifically Pocilloporids, to climate change and ocean warming in Australia has varied by region. For example, bleaching events occurring on the tropical reefs of the Great Barrier Reef have impacted almost all species (Stuart-Smith et al., 2018), with over 43% of reefs bleaching in 1998, 56% bleaching in 2002, and 85% in 2016 (Hughes et al., 2017) and region-wide coral bleaching occurring from February–April 2020 and December–March 2022 (Ainsworth et al., 2021, GBRMPA Reef Snapshot, 2022). Pocillopora spp. has been categorised as bleaching-sensitive on the GBR, showing declines in small colonies of up to 28% on the reef crest and 30.2% on the reef slope following mass coral bleaching in 2016/2017 (Dietzel et al., 2020). In the Keppel Island archipelago, situated on the southern inshore GBR, 21% of living corals were affected by bleaching, with Pocillopora and branching Acropora the most affected (Kennedy et al., 2017). Botté et al. (2022) also found a degree of mild, moderate, or severe bleaching in all Pocillopora acuta colonies sampled between 3.5–5.6°C-weeks on Pandora and Havannah Island reefs within the Palm Island group on the central GBR. However, in the Coral Sea, partial mortality was lower in Pocillopora species during bleaching in 2020 than in 2018/2019 prior to bleaching, and overall incidence of partial mortality in all species surveyed remained below 5% (Burn et al., 2022). Outside of Australia, co-evolved mutualisms between Pocillopora corals and heat-tolerant symbionts have been found with few observable tradeoffs, suggesting that increased prevalence of these mutualisms will contribute to reef growth and the proliferation of Pocillopora spp. in warming environments (Mexico; Turnham et al., 2023). An additional study in Panama suggests that Pocillopora will be selected over other coral genera in warming regions, due to associations with thermotolerant symbionts, the potential acquisition of thermally tolerant symbionts during heat stress, and generalist traits such as a high growth rate and capacity for asexual reproduction through fragmentation (Palacio-Castro et al., 2023). However, in an Australian context, dominance of Pocilloporids on Australia’s reefs will come with a reduction in non-Pocilloporid species in a formerly highly diverse region. This reduction in non-Pocilloporid species diversity may impact ecological functions and reef resilience to other stressors in highly variable, marginal environments.
In subtropical or marginal reefs, such as those around Norfolk Island and Lord Howe Island, the reefs are dominated by subtropical and temperate species and presumed to be isolated from surrounding bioregions. This creates a unique environment with a high presence of endemic fauna and peripheral populations vulnerable to extinction (van der Meer et al., 2015; Edgar et al., 2017). However, there has been limited research to date focused on coral populations in these subtropical environments, and how generalist species and the overall coral populations will be affected by warming oceans is largely unknown. At Lord Howe Island between 2005 and 2007 up to 95% of the coral community in the lagoon bleached, with 41% mortality occurring in Pocillopora damicornis as well as evidence of minor bleaching in Poritidae and Acroporidae (Dalton et al., 2011). In 2010, 2011 and 2019, bleaching was also observed in lagoonal sites at Lord Howe Island, with up to 99% of colonies bleached at shallow lagoon sites and Pocillopora, Stylophora, Seriatopora, and Porites as the most affected species (Dalton et al., 2020). The responses of Pocilloporids to warming are clearly variable across environments.
In temperate reefs, such as the continental coral reefs of the eastern extent of the Great Southern Reef (GSR) including the Solitary Islands Marine Park (SIMP) and the associated reefs of Australia’s southeast coast, ocean warming is contributing to range contractions, habitat losses, changes in energy pathways, and the facilitation of species (Wernberg et al., 2013; Vergés et al., 2014; Tuckett et al., 2017; Smith et al., 2021). In surveys of a bleaching event extending along the eastern coast of Australia from Flinders Reef to Southwest Rocks (including the SIMP), Pocillopora bleached more at sites where temperatures were historically cooler and overall, Pocillopora and Porites were more susceptible to bleaching than Acropora, Goniastrea, and Turbinaria (Kim et al., 2019). Bleaching severity also increased for Pocillopora spp. with latitude without a significant change in relative abundance (Kim et al., 2019). Abrupt changes to the size structure of the endemic Pocillopora aliciae were also noted following a bleaching event in 2016, demonstrating a strong association between heat stress and declining P. aliciae population density (Lachs et al., 2021). P. aliciae is a subtropical endemic branching coral (Schmidt-Roach et al., 2013a; Schmidt-Roach et al., 2013b; Schmidt-Roach et al., 2014), which is hypothesised to have extended its range into temperate (18.8–24.7°C 2012–2022 monthly average) habitats of Sydney NSW (Booth and Sear, 2018). Establishment of P. aliciae in temperate waterways has been suggested to accelerate tropicalization of coastal Sydney and facilitate benthic habitat complexity for fish communities, although further examination is needed to determine the limits of coral range extension into high-latitude regions (Abrego et al., 2021). However, despite generally exhibiting an enhanced stress tolerance characteristic of corals in a fluctuating environment (Oliver and Palumbi, 2011), P. aliciae has been deemed the least viable coral species under thermal stress at the SIMP (Cant et al., 2021) and is categorised as susceptible to thermal stress.
This is further evident with the 2016 El Niño and a corresponding increase in seawater temperatures of > 2°C above the long-term mean summer maxima causing bleaching in up to 60% of all corals in Sydney Harbour (Goyen et al., 2019). Incorporating the response of Pocilloporid species under thermal stress into the response of the benthic coral community as a whole, there is evidence of an overall decline in total coral cover at the SIMP between 1990 and 2014 (Mizerek et al., 2021). Taken together, these studies suggest that the response of Pocilloporid species to thermal stress within the reefs of eastern Australia are still equivocal and highly variable by region, and likely depend on location-specific adaptations.
5 Conclusion
Community reassembly, altered dispersal patterns, and novel species interactions, including novel holobiont–environment interactions, are hypothesised to be involved in the formation of entirely novel ecosystems (Spalding et al., 2007; Sommer et al., 2014; Sommer et al., 2017; Sommer et al., 2018). Ocean warming is hypothesised to warm regions considered marginal environments for coral growth and expand coral dominance in these locations (Beger et al., 2014; Tuckett et al., 2017; Booth and Sear, 2018; Nakabayashi et al., 2019; González-Pech et al., 2022). As such, recent studies have focused on how ocean warming may drive the development of novel coral ecosystems in high-latitude reef habitats, described as “changes in species configurations, interactions, and functions, within the parameter space of calcifying coral-dominated reefs” (Graham et al., 2014).
However, warming is also driving marine heatwaves and bleaching events, as seen in the past decades across Australia’s subtropical and temperate reef systems and coral populations. In Australia alone, coral bleaching has been observed in high-latitude locations within the last two decades with a frequency and severity comparable to that of tropical locations. In Australia bleaching events have been reported at Lord Howe Island (Harrison et al., 2011; Dalton et al., 2020), Rottnest Island (Thomson et al., 2011; le Nohaïc et al., 2017), eastern New South Wales (Kim et al., 2019), Sydney Harbour (Goyen et al., 2019), and the Houtman Abrolhos Islands (Abdo et al., 2012; Smale et al., 2012). One of the most extreme examples of changing distribution is the expansion of the coral Pocillopora aliciae into temperate marine environments close to Sydney Harbour (González-Pech et al., 2022). It is therefore critical to understand which coral species, in which locations and by which means, are functioning as generalists as these species are predicted to be better able to withstand a changing environment. Generalist species may provide new ecological opportunities and play critical functional roles as coral reefs reconfigure under climate change. More research is warranted to define generalist traits and which species display them.
Author contributions
JB reviewed the literature and wrote the manuscript with contribution from TA, PS, and ZR. All authors contributed to the article and approved the submitted version.
Funding
This project was supported by a UNSW Scientia Scholarship, Australian Government Research Training Program Scholarship, and the American Australian Association’s Graduate Education Fund Scholarship to JB. In addition, TA was supported by UNSW Scientia Funding and research conducted with Parks Australia.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher’s note
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Keywords: generalist, coral reefs, climate change, Pocilloporid, Australia
Citation: Bergman JL, Richards ZT, Sawyers P and Ainsworth TD (2023) Environmental generalism, holobiont interactions, and Pocilloporid corals in the warming oceans of the eastern coast of Australia. Front. Ecol. Evol. 11:1190455. doi: 10.3389/fevo.2023.1190455
Received: 20 March 2023; Accepted: 28 November 2023;
Published: 18 December 2023.
Edited by:
Jennifer L. Matthews, University of Technology Sydney, AustraliaReviewed by:
Alexandra Dempsey, Khaled bin Sultan Living Oceans Foundation, United StatesYvonne Sawall, Bermuda Institute of Ocean Sciences, Bermuda
Copyright © 2023 Bergman, Richards, Sawyers and Ainsworth. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Jessica L. Bergman, j.bergman@unsw.edu.au