Douglas B. Rasher

Chemically rich seaweeds poison corals when not controlled by herbivores.

Coral reefs are in dramatic global decline, with seaweeds commonly replacing corals. It is unclear, however, whether seaweeds harm corals directly or colonize opportunistically following their decline and then suppress coral recruitment. In the Caribbean and tropical Pacific, we show that, when protected from herbivores, ~40 to 70% of common seaweeds cause bleaching and death of coral tissue when in direct contact. For seaweeds that harmed coral tissues, their lipid-soluble extracts also produced rapid bleaching. Coral bleaching and mortality was limited to areas of direct contact with seaweeds or their extracts. These patterns suggest that allelopathic seaweed-coral interactions can be important on reefs lacking herbivore control of seaweeds, and that these interactions involve lipid-soluble metabolites transferred via direct contact. Seaweeds were rapidly consumed when placed on a Pacific reef protected from fishing but were left intact or consumed at slower rates on an adjacent fished reef, indicating that herbivory will suppress seaweeds and lower frequency of allelopathic damage to corals if reefs retain intact food webs. With continued removal of herbivores from coral reefs, seaweeds are becoming more common. This occurrence will lead to increasing frequency of seaweed-coral contacts, increasing allelopathic suppression of remaining corals, and continuing decline of reef corals.

Consumer diversity interacts with prey defenses to drive ecosystem function.

Prey traits linking consumer diversity to ecosystem function remain poorly understood. On tropical coral reefs, herbivores promote coral dominance by suppressing competing macroalgae, but the roles of herbivore identity and diversity, macroalgal defenses, and their interactions in affecting reef resilience and function are unclear. We studied adjacent pairs of no-take marine reserves and fished areas on reefs in Fiji and found that protected reefs supported 7-17x greater biomass, 2-3x higher species richness of herbivorous fishes, and 3-11x more live coral cover than did fished reefs. In contrast, macroalgae were 27-61x more abundant and 3-4x more species-rich on fished reefs. When we transplanted seven common macroalgae from fished reefs into reserves they were rapidly consumed, suggesting that rates of herbivory (ecosystem functioning) differed inside vs. outside reserves. We then video-recorded feeding activity on the same seven macroalgae when transplanted into reserves, and assessed the functional redundancy vs. complementarity of herbivorous fishes consuming these macroalgae. Of 29 species of larger herbivorous fishes on these reefs, only four species accounted for 97% of macroalgal consumption. Two unicornfish consumed a range of brown macroalgae, a parrotfish consumed multiple red algae, and a rabbitfish consumed a green alga, with almost no diet overlap among these groups. The two most chemically rich, allelopathic algae were each consumed by a single, but different, fish species. This striking complementarity resulted from herbivore species differing in their tolerances to macroalgal chemical and structural defenses. A model of assemblage diet breadth based on our feeding observations predicted that high browser diversity would be required for effective control of macroalgae on Fijian reefs. In support of this model, we observed strong negative relationships between herbivore diversity and macroalgal abundance and diversity across the six study reefs. Our findings indicate that the total diet breadth of the herbivore community and the probability of all macroalgae being removed from reefs by herbivores increases with increasing herbivore diversity, but that a few critical species drive this relationship. Therefore, interactions between algal defenses and herbivore tolerances create an essential role for consumer diversity in the functioning and resilience of coral reefs.

Macroalgal terpenes function as allelopathic agents against reef corals

During recent decades, many tropical reefs have transitioned from coral to macroalgal dominance. These community shifts increase the frequency of algal–coral interactions and may suppress coral recovery following both anthropogenic and natural disturbance. However, the extent to which macroalgae damage corals directly, the mechanisms involved, and the species specificity of algal–coral interactions remain uncertain. Here, we conducted field experiments demonstrating that numerous macroalgae directly damage corals by transfer of hydrophobic allelochemicals present on algal surfaces. These hydrophobic compounds caused bleaching, decreased photosynthesis, and occasionally death of corals in 79% of the 24 interactions assayed (three corals and eight algae). Coral damage generally was limited to sites of algal contact, but algae were unaffected by contact with corals. Artificial mimics for shading and abrasion produced no impact on corals, and effects of hydrophobic surface extracts from macroalgae paralleled effects of whole algae; both findings suggest that local effects are generated by allelochemical rather than physical mechanisms. Rankings of macroalgae from most to least allelopathic were similar across the three coral genera tested. However, corals varied markedly in susceptibility to allelopathic algae, with globally declining corals such as Acropora more strongly affected. Bioassay-guided fractionation of extracts from two allelopathic algae led to identification of two loliolide derivatives from the red alga Galaxaura filamentosa and two acetylated diterpenes from the green alga Chlorodesmis fastigiata as potent allelochemicals. Our results highlight a newly demonstrated but potentially widespread competitive mechanism to help explain the lack of coral recovery on many present-day reefs.

Competition induces allelopathy but suppresses growth and anti-herbivore defence in a chemically rich seaweed

Many seaweeds and terrestrial plants induce chemical defences in response to herbivory, but whether they induce chemical defences against competitors (allelopathy) remains poorly understood. We evaluated whether two tropical seaweeds induce allelopathy in response to competition with a reef-building coral. We also assessed the effects of competition on seaweed growth and seaweed chemical defence against herbivores. Following 8 days of competition with the coral Porites cylindrica, the chemically rich seaweed Galaxaura filamentosa induced increased allelochemicals and became nearly twice as damaging to the coral. However, it also experienced significantly reduced growth and increased palatability to herbivores (because of reduced chemical defences). Under the same conditions, the seaweed Sargassum polycystum did not induce allelopathy and did not experience a change in growth or palatability. This is the first demonstration of induced allelopathy in a seaweed, or of competitors reducing seaweed chemical defences against herbivores. Our results suggest that the chemical ecology of coral–seaweed–herbivore interactions can be complex and nuanced, highlighting the need to incorporate greater ecological complexity into the study of chemical defence.

Seaweed allelopathy degrades the resilience and function of coral reefs

Coral reefs are in dramatic global decline due to a host of local- and global-scale anthropogenic disturbances that suppress corals and enhance seaweeds. This decline is exacerbated, and recovery made less likely, due to overfishing of herbivores that normally limit seaweed effects on corals. Seaweeds were known to suppress coral reproduction and recruitment, but in a recent study, we demonstrated that numerous seaweeds also directly poison corals via lipid-soluble allelochemicals transferred during contact. These allelopathic interactions may limit reef recovery once seaweeds proliferate and commonly contact remaining corals. Other recent studies suggest that seaweeds may also damage corals by enhancing coral disease or via release of water-soluble organics than stimulate damaging microbes. For some of these mechanisms, cause versus effect is not yet clear. Here, we suggest that these different mechanisms are not mutually exclusive, may interact in context-dependent ways, but need to be assessed under ecologically realistic field conditions where flow may limit impacts of some mechanisms.

Marine and terrestrial herbivores display convergent chemical ecology despite 400 million years of independent evolution

Significance We report, for the first time to our knowledge, compounds that specialist marine herbivores use to find their prey. The seaweed Halimeda incrassata produces metabolites that deter feeding by generalist herbivores. However, a specialist sea slug, Elysia tuca, follows these defensive compounds and not only attacks the seaweed but does so preferentially while the seaweed is reproducing. Elysia sequester Halimeda’s chemical defenses (to deter predators) and chloroplasts (becoming photosynthetic). Elysia feeding reduces Halimeda growth by ∼50%, but the alga drops branches occupied by Elysia, possibly to avoid fungal infection associated with herbivory and to rid itself of Elysia. These interactions parallel many involving terrestrial insects and plants, even though marine and terrestrial herbivores have evolved independently for 400 million years. Chemical cues regulate key ecological interactions in marine and terrestrial ecosystems. They are particularly important in terrestrial plant–herbivore interactions, where they mediate both herbivore foraging and plant defense. Although well described for terrestrial interactions, the identity and ecological importance of herbivore foraging cues in marine ecosystems remain unknown. Here we show that the specialist gastropod Elysia tuca hunts its seaweed prey, Halimeda incrassata, by tracking 4-hydroxybenzoic acid to find vegetative prey and the defensive metabolite halimedatetraacetate to find reproductive prey. Foraging cues were predicted to be polar compounds but instead were nonpolar secondary metabolites similar to those used by specialist terrestrial insects. Tracking halimedatetraacetate enables Elysia to increase in abundance by 12- to 18-fold on reproductive Halimeda, despite reproduction in Halimeda being rare and lasting for only ∼36 h. Elysia swarm to reproductive Halimeda where they consume the alga’s gametes, which are resource rich but are chemically defended from most consumers. Elysia sequester functional chloroplasts and halimedatetraacetate from Halimeda to become photosynthetic and chemically defended. Feeding by Elysia suppresses the growth of vegetative Halimeda by ∼50%. Halimeda responds by dropping branches occupied by Elysia, apparently to prevent fungal infection associated with Elysia feeding. Elysia is remarkably similar to some terrestrial insects, not only in its hunting strategy, but also its feeding method, defense tactics, and effects on prey behavior and performance. Such striking parallels indicate that specialist herbivores in marine and terrestrial systems can evolve convergent ecological strategies despite 400 million years of independent evolution in vastly different habitats.

Coral reefs in crisis: reversing the biotic death spiral.

Coral reefs are disappearing due to global warming, overfishing, ocean acidification, pollution, and interactions of these and other stresses. Ecologically informed management of fishes that facilitate corals by suppressing seaweeds may be our best bet for bringing reefs back from the brink of extinction.

Cascading predator effects in a Fijian coral reef ecosystem

Coral reefs are among Earth’s best-studied ecosystems, yet the degree to which large predators influence the ecology of coral reefs remains an open and contentious question. Recent studies indicate the consumptive effects of large reef predators are too diffuse to elicit trophic cascades. Here, we provide evidence that such predators can produce non-consumptive (fear) effects that flow through herbivores to shape the distribution of seaweed on a coral reef. This trophic cascade emerged because reef topography, tidal oscillations, and shark hunting behaviour interact to create predictable “hot spots” of fear on the reef where herbivores withhold feeding and seaweeds gain a spatial refuge. Thus, in risky habitats, sharks can exert strong ecological impacts even though they are trophic generalists that rarely feed. These findings contextualize the debate over whether predators influence coral reef structure and function and move us to ask not if, but under what specific conditions, they generate trophic cascades.

Spatial and temporal limits of coral-macroalgal competition: the negative impacts of macroalgal density, proximity, and history of contact

Tropical reefs are commonly transitioning from coral- to macroalgal-dominance, producing abrupt, and often lasting, shifts in community composition and ecosystem function. Although negative effects of macroalgae on corals are well documented, whether such effects vary with spatial scale or the density of macroalgae remains inadequately understood, as does the legacy of their impact on coral growth. Using closely adjacent coral- versus macroalgal-dominated areas, we tested effects of macroalgal competition on the Indo-Pacific corals Acropora millepora and Porites cylindrica. When corals were transplanted to areas of: i) macroalgal-dominance, ii) macroalgal-dominance but with nearby macroalgae removed, or iii) coral-dominance lacking macroalgae, coral growth was equivalently high in plots without macroalgae and low (62-90% less) in plots with macroalgae, regardless of location. In a separate experiment, we raised corals above the benthos in each area and exposed them to differing densities of the dominant macroalga Sargassum polycystum. Coral survivorship was high (≥ 93% after 3 months) and did not differ among treatments, whereas the growth of both coral species decreased as a function of Sargassum density. When Sargassum was removed after two months, there was no legacy effect of macroalgal density on coral growth over the next seven months; however, there was no compensation for previously depressed growth. In sum, macroalgal impacts were density dependent, occurred only if macroalgae were in close contact, and coral growth was resilient to prior macroalgal contact. The temporal and spatial constraints of these interactions suggest that corals may be surprisingly resilient to periodic macroalgal competition, which could have important implications for ecosystem trajectories that lead to reef decline or recovery.

Attenuating effects of ecosystem management on coral reefs

Local management improves coral reef’s capacity to recover from disturbances, but the signal attenuates unless properly measured. Managing diverse ecosystems is challenging because structuring drivers are often processes having diffuse impacts that attenuate from the people who were “managed” to the expected ecosystem-wide outcome. Coral reef fishes targeted for management only indirectly link to the ecosystem’s foundation (reef corals). Three successively weakening interaction tiers separate management of fishing from coral abundance. We studied 12 islands along the 700-km eastern Caribbean archipelago, comparing fished and unfished coral reefs. Fishing reduced biomass of carnivorous (snappers and groupers) and herbivorous (parrotfish and surgeonfish) fishes. We document attenuating but important effects of managing fishing, which explained 37% of variance in parrotfish abundance, 20% of variance in harmful algal abundance, and 17% of variance in juvenile coral abundance. The explained variance increased when we quantified herbivory using area-specific bite rates. Local fisheries management resulted in a 62% increase in the archipelago’s juvenile coral density, improving the ecosystem’s recovery potential from major disturbances.