storms are also major drivers of coral loss in some reef systems, including the Great
Barrier Reef (Lam et al. 2018). More recently, ocean hypoxia, due to warming and
nutrient pollution, has emerged as possibly the most imminent threat to corals
(Hughes et al. 2020). In the end-Permian biotic crisis, which saw losses of up to
96% of marine species, temperature-dependent hypoxia was likely the major cause
of most extinctions (Penn et al. 2018). Ocean acidification also reduces the rate of
skeleton formation of stony corals and other organisms that produce calcium carbonate skeletons or shells (Hoegh-Guldberg et al. 2007).
Corals have exhibited limited resilience to these anthropogenic stressors, which
act in negative synergy, with responses derived from the animals as well as the
symbionts (Carballo-Bolanos et al. 2020; Apprill 2020). Besides temporary switches
to heterotrophy (Grottoli et al. 2006), corals can exhibit acclimatization. For example, thermal preconditioning, even without shifts in symbionts, can reduce susceptibility to bleaching (Bellantuono et al. 2012). Can corals adapt? While heritable
variation in thermal tolerance in corals has been documented (Dixon et al. 2015),
4–8 year sexual generation times imply a limited capability for rapid adaptation.
Instead, resilience is more likely to emerge from partnering symbionts. The environmentally acquired Symbiodiniaceae taxa associating with corals vary considerably in thermal tolerance and hence provide opportunities for symbiont switching.
After bleaching events, more thermally tolerant symbionts, including Durusdinium
species (clade D in the A-I scheme), can replace less tolerant species. This can lead to
shifts in the relative abundance of specific community members or complete symbiont replacement (Boulotte et al. 2016). Symbiont switching, however, may offer
only a temporary reprieve depending on the amount of warming, or not be an option
for some species. For instance, corals living in the Persian Gulf, among the warmest
regions, appear inflexible to changing partners, possibly because they already
associate with the most tolerant partners (Howells et al. 2020). Moreover, some
coral-symbiont associations appear more coevolved, which may make partner swapping a less viable strategy (Tamar 2006; Stat et al. 2009). Since symbionts have
much faster replication times than their hosts they are more likely to adapt to rapidly
changing conditions. Genetic variations in nutrient and thermal tolerance are known
for photosymbionts, and rapid adaptation in the laboratory has been documented
(Chakravarti et al. 2017; Bayliss et al. 2019), but it remains unclear whether
symbiont adaptation will play key resilience roles in natural systems.
About a quarter of corals are “depth generalists” suggesting some diversity may
be maintained in “deep reef refugia” (Bongaerts et al. 2010). Recently, 13% of
shallow-reef (<30 m) hard coral species associated with the Great Barrier Reef were
unexpectedly found at depths below 45 m (Muir et al. 2018). Similarly, thermalresistant corals from warm bodies of water may also persist and even be used in
ecological restoration efforts (Morikawa and Palumbi 2019). In summary, corals and
the diverse biotic and human communities they support are in deep trouble. While
symbiont replacement, adaptation or relocation may provide a temporary or partial
reprieve, expected atmospheric warming in the coming decades is predicted to result
in the loss of more than 99% of the world’s reefs (IPCC 2018). Climate-mediated
bleaching will similarly challenge other photosymbiotic animals, including already
16 Symbiosis in a Rapidly Changing World
271
Barrier Reef (Lam et al. 2018). More recently, ocean hypoxia, due to warming and
nutrient pollution, has emerged as possibly the most imminent threat to corals
(Hughes et al. 2020). In the end-Permian biotic crisis, which saw losses of up to
96% of marine species, temperature-dependent hypoxia was likely the major cause
of most extinctions (Penn et al. 2018). Ocean acidification also reduces the rate of
skeleton formation of stony corals and other organisms that produce calcium carbonate skeletons or shells (Hoegh-Guldberg et al. 2007).
Corals have exhibited limited resilience to these anthropogenic stressors, which
act in negative synergy, with responses derived from the animals as well as the
symbionts (Carballo-Bolanos et al. 2020; Apprill 2020). Besides temporary switches
to heterotrophy (Grottoli et al. 2006), corals can exhibit acclimatization. For example, thermal preconditioning, even without shifts in symbionts, can reduce susceptibility to bleaching (Bellantuono et al. 2012). Can corals adapt? While heritable
variation in thermal tolerance in corals has been documented (Dixon et al. 2015),
4–8 year sexual generation times imply a limited capability for rapid adaptation.
Instead, resilience is more likely to emerge from partnering symbionts. The environmentally acquired Symbiodiniaceae taxa associating with corals vary considerably in thermal tolerance and hence provide opportunities for symbiont switching.
After bleaching events, more thermally tolerant symbionts, including Durusdinium
species (clade D in the A-I scheme), can replace less tolerant species. This can lead to
shifts in the relative abundance of specific community members or complete symbiont replacement (Boulotte et al. 2016). Symbiont switching, however, may offer
only a temporary reprieve depending on the amount of warming, or not be an option
for some species. For instance, corals living in the Persian Gulf, among the warmest
regions, appear inflexible to changing partners, possibly because they already
associate with the most tolerant partners (Howells et al. 2020). Moreover, some
coral-symbiont associations appear more coevolved, which may make partner swapping a less viable strategy (Tamar 2006; Stat et al. 2009). Since symbionts have
much faster replication times than their hosts they are more likely to adapt to rapidly
changing conditions. Genetic variations in nutrient and thermal tolerance are known
for photosymbionts, and rapid adaptation in the laboratory has been documented
(Chakravarti et al. 2017; Bayliss et al. 2019), but it remains unclear whether
symbiont adaptation will play key resilience roles in natural systems.
About a quarter of corals are “depth generalists” suggesting some diversity may
be maintained in “deep reef refugia” (Bongaerts et al. 2010). Recently, 13% of
shallow-reef (<30 m) hard coral species associated with the Great Barrier Reef were
unexpectedly found at depths below 45 m (Muir et al. 2018). Similarly, thermalresistant corals from warm bodies of water may also persist and even be used in
ecological restoration efforts (Morikawa and Palumbi 2019). In summary, corals and
the diverse biotic and human communities they support are in deep trouble. While
symbiont replacement, adaptation or relocation may provide a temporary or partial
reprieve, expected atmospheric warming in the coming decades is predicted to result
in the loss of more than 99% of the world’s reefs (IPCC 2018). Climate-mediated
bleaching will similarly challenge other photosymbiotic animals, including already
16 Symbiosis in a Rapidly Changing World
271