Biodiversity of macroalgae does not differentially suppress coral performance: The other side of a biodiversity issue.

Hundreds of studies now document positive relationships between biodiversity and critical ecosystem processes, but as ecological communities worldwide shift toward new species configurations, less is known regarding how the biodiversity of undesirable species will shape the functioning of ecosystems or foundation species. We manipulated macroalgal species richness in experimental field plots to test whether and how the identity and diversity of competing macroalgae affected the growth, survival, and microbiome of a common coral in Mo'orea, French Polynesia. Compared to controls without algal competitors, coral growth was significantly suppressed across three macroalgal monocultures, a polyculture of the same three macroalgae, and plots containing inert seaweed mimics; coral mortality was limited and did not differ significantly among treatments. One macroalga suppressed coral growth significantly less than the other two, but none differed from the inert mimic in terms of coral suppression. The composition, dispersion, and diversity of coral microbiomes in treatments with live macroalgae or inert plastic mimics did not differ from controls experiencing no competition. Microbiome composition differed between two macroalgal monocultures and a monoculture versus plastic mimics, but no other microbiome differences were observed among macroalgal or mimic treatments. Together, these findings suggest that algal diversity does not alter harmful impacts of macroalgae on coral performance, which could be accounted for by physical structure alone in these field experiments. While enhancing biodiversity is a recognized strategy for promoting desirable species, it would be worrisome if biodiversity also enhanced the negative impacts of undesirable species. We documented no such effects in this investigation.

Removal of detritivore sea cucumbers from reefs increases coral disease.

Coral reefs are in global decline with coral diseases playing a significant role. This is especially true for Acroporid corals that represent ~25% of all Pacific coral species and generate much of the topographic complexity supporting reef biodiversity. Coral diseases are commonly sediment-associated and could be exacerbated by overharvest of sea cucumber detritivores that clean reef sediments and may suppress microbial pathogens as they feed. Here we show, via field manipulations in both French Polynesia and Palmyra Atoll, that historically overharvested sea cucumbers strongly suppress disease among corals in contact with benthic sediments. Sea cucumber removal increased tissue mortality of Acropora pulchra by ~370% and colony mortality by ~1500%. Additionally, farmerfish that kill Acropora pulchra bases to culture their algal gardens further suppress disease by separating corals from contact with the disease-causing sediment-functioning as mutualists rather than parasites despite killing coral bases. Historic overharvesting of sea cucumbers increases coral disease and threatens the persistence of tropical reefs. Enhancing sea cucumbers may enhance reef resilience by suppressing disease.

Historic trophic decline in New England's coastal marine ecosystem.

Overfishing is a worldwide occurrence that simplifies marine food webs, changes trophic patterns, and alters community structure, affecting not only the density of harvested species but also their trophic function. The northwestern Atlantic has a history of heavy fishing, and over the past century has also experienced destructive bottom fishing and harmful mobile fishing gear. After confirming that preservation solvent did not alter the nitrogen stable isotopes of preserved samples, we used museum specimens and modern samples to analyze nitrogen stable isotopes in tissues of two common demersal fishes pre-1950 (1850 to 1950) compared to 2021 to assess changes in trophic positions of coastal New England consumers over this time period. Both the mesopredator Centropristis striata (black sea bass) and the benthivore Stenotomus chrysops (scup) experienced significant declines in trophic position during this time. C. striata declined almost a full trophic level, S. chrysops declined half a trophic level, and these species are now occupying almost the same trophic position. Heavy fishing activities potentially shorten food chains, simplify trophic complexity, lessen the separation of trophic niches, and generally flatten food webs. The consequences of these within-species shifts are poorly investigated but could generate underappreciated cascading impacts on community structure and function. Archived natural-history collections are an invaluable resource for investigating ecological changes in natural communities through time. The evaluation of changing trophic positions via stable isotope analysis may allow fisheries managers to quantify large-scale effects of fishing on ecosystems and food webs over time.

Biodiversity has a positive but saturating effect on imperiled coral reefs.

Species loss threatens ecosystems worldwide, but the ecological processes and thresholds that underpin positive biodiversity effects among critically important foundation species, such as corals on tropical reefs, remain inadequately understood. In field experiments, we manipulated coral species richness and intraspecific density to test whether, and how, biodiversity affects coral productivity and survival. Corals performed better in mixed species assemblages. Improved performance was unexplained by competition theory alone, suggesting that positive effects exceeded agonistic interactions during our experiments. Peak coral performance occurred at intermediate species richness and declined thereafter. Positive effects of coral diversity suggest that species' losses on degraded reefs make recovery more difficult and further decline more likely. Harnessing these positive interactions may improve ecosystem conservation and restoration in a changing ocean.

Human proximity suppresses fish recruitment by altering mangrove-associated odour cues.

Human-driven threats to coastal marine communities could potentially affect chemically mediated behaviours that have evolved to facilitate crucial ecological processes. Chemical cues and their importance remain inadequately understood in marine systems, but cues from coastal vegetation can provide sensory information guiding aquatic animals to key resources or habitats. In the tropics, mangroves are a ubiquitous component of healthy coastal ecosystems, associated with a range of habitats from river mouths to coral reefs. Because mangrove leaf litter is a predictable cue to coastal habitats, chemical information from mangrove leaves could provide a source of settlement cues for coastal fishes, drawing larvae towards shallow benthic habitats or inducing settlement. In choice assays, juvenile fishes from the Caribbean (Belize) and Indo-Pacific (Fiji) were attracted to cues from mangroves leaves and were more attracted to cues from mangroves distant from human settlement. In the field, experimental reefs supplemented with mangrove leaves grown away from humans attracted more fish recruits from a greater diversity of species than reefs supplemented with leaves grown near humans. Together, this suggests that human use of coastal areas alters natural chemical cues, negatively affecting the behavioural responses of larval fishes and potentially suppressing recruitment. Overall, our findings highlight the critical links that exist between marine and terrestrial habitats, and the importance of considering these in the broader conservation and management of coastal ecosystems.

Trophic interactions will expand geographically but be less intense as oceans warm.

Interactions among species are likely to change geographically due to climate-driven species range shifts and in intensity due to physiological responses to increasing temperatures. Marine ectotherms experience temperatures closer to their upper thermal limits due to the paucity of temporary thermal refugia compared to those available to terrestrial organisms. Thermal limits of marine ectotherms also vary among species and trophic levels, making their trophic interactions more prone to changes as oceans warm. We assessed how temperature affects reef fish trophic interactions in the Western Atlantic and modeled projections of changes in fish occurrence, biomass, and feeding intensity across latitudes due to climate change. Under ocean warming, tropical reefs will experience diminished trophic interactions, particularly herbivory and invertivory, potentially reinforcing algal dominance in this region. Tropicalization events are more likely to occur in the northern hemisphere, where feeding by tropical herbivores is predicted to expand from the northern Caribbean to extratropical reefs. Conversely, feeding by omnivores is predicted to decrease in this area with minor increases in the Caribbean and southern Brazil. Feeding by invertivores declines across all latitudes in future predictions, jeopardizing a critical trophic link. Most changes are predicted to occur by 2050 and can significantly affect ecosystem functioning, causing dominance shifts and the rise of novel ecosystems.

Effects of future climate on coral-coral competition.

As carbon dioxide (CO2) levels increase, coral reefs and other marine systems will be affected by the joint stressors of ocean acidification (OA) and warming. The effects of these two stressors on coral physiology are relatively well studied, but their impact on biotic interactions between corals are poorly understood. While coral-coral interactions are less common on modern reefs, it is important to document the nature of these interactions to better inform restoration strategies in the face of climate change. Using a mesocosm study, we evaluated whether the combined effects of ocean acidification and warming alter the competitive interactions between the common coral Porites astreoides and two other mounding corals (Montastraea cavernosa or Orbicella faveolata) common in the Caribbean. After 7 days of direct contact, P. astreoides suppressed the photosynthetic potential of M. cavernosa by 100% in areas of contact under both present (~28.5°C and ~400 µatm pCO2) and predicted future (~30.0°C and ~1000 µatm pCO2) conditions. In contrast, under present conditions M. cavernosa reduced the photosynthetic potential of P. astreoides by only 38% in areas of contact, while under future conditions reduction was 100%. A similar pattern occurred between P. astreoides and O. faveolata at day 7 post contact, but by day 14, each coral had reduced the photosynthetic potential of the other by 100% at the point of contact, and O. faveolata was generating larger lesions on P. astreoides than the reverse. In the absence of competition, OA and warming did not affect the photosynthetic potential of any coral. These results suggest that OA and warming can alter the severity of initial coral-coral interactions, with potential cascading effects due to corals serving as foundation species on coral reefs.

Caribbean reefs of the Anthropocene: Variance in ecosystem metrics indicates bright spots on coral depauperate reefs.

Dramatic coral loss has significantly altered many Caribbean reefs, with potentially important consequences for the ecological functions and ecosystem services provided by reef systems. Many studies examine coral loss and its causes-and often presume a universal decline of ecosystem services with coral loss-rather than evaluating the range of possible outcomes for a diversity of ecosystem functions and services at reefs varying in coral cover. We evaluate 10 key ecosystem metrics, relating to a variety of different reef ecosystem functions and services, on 328 Caribbean reefs varying in coral cover. We focus on the range and variability of these metrics rather than on mean responses. In contrast to a prevailing paradigm, we document high variability for a variety of metrics, and for many the range of outcomes is not related to coral cover. We find numerous "bright spots," where herbivorous fish biomass, density of large fishes, fishery value, and/or fish species richness are high, despite low coral cover. Although it remains critical to protect and restore corals, understanding variability in ecosystem metrics among low-coral reefs can facilitate the maintenance of reefs with sustained functions and services as we work to restore degraded systems. This framework can be applied to other ecosystems in the Anthropocene to better understand variance in ecosystem service outcomes and identify where and why bright spots exist.

Seaweed-coral competition in the field: effects on coral growth, photosynthesis and microbiomes require direct contact.

A number of tropical reefs have transitioned from coral to macroalgal dominance, but the role of macroalgal competition in coral decline is debated. There is a need to understand the relative roles of direct coral-algal effects versus indirect, microbially mediated effects shaping these interactions, as well as the relevant scales at which interactions operate under natural field, as opposed to laboratory, conditions. We conducted a manipulative field experiment investigating how direct contact versus close proximity (approx. 1.5 cm) with macroalgae (Galaxaura rugosa, Sargassum polycystum) impacted the growth, photosynthetic efficiency, and prokaryotic microbiome of the common Indo-Pacific coral Acropora millepora. Both coral growth and photosynthetic efficiency were suppressed when in direct contact with algae or their inert mimics--but not when in close proximity to corals without direct contact. Coral microbiomes were largely unaltered in composition, variability, or diversity regardless of treatment, although a few uncommon taxa differed in abundance among treatments. Negative impacts of macroalgae were contact dependent, accounted for by physical structure alone and had minimal effects on coral microbiomes. The spatial constraints of these interactions have important implications for understanding and predicting benthic community dynamics as reefs degrade.

Parasite-host ecology: the limited impacts of an intimate enemy on host microbiomes.

BACKGROUND: Impacts of biotic stressors, such as consumers, on coral microbiomes have gained attention as corals decline worldwide. Corallivore feeding can alter coral microbiomes in ways that contribute to dysbiosis, but feeding strategies are diverse - complicating generalizations about the nature of consumer impacts on coral microbiomes. RESULTS: In field experiments, feeding by Coralliophila violacea, a parasitic snail that suppresses coral growth, altered the microbiome of its host, Porites cylindrica, but these impacts were spatially constrained. Alterations in microbial community composition and variability were largely restricted to snail feeding scars; basal or distal areas ~ 1.5 cm or 6-8 cm away, respectively, were largely unaltered. Feeding scars were enriched in taxa common to stressed corals (e.g. Flavobacteriaceae, Rhodobacteraceae) and depauperate in putative beneficial symbionts (e.g. Endozoicomonadaceae) compared to locations that lacked feeding. CONCLUSIONS: Previous studies that assessed consumer impacts on coral microbiomes suggested that feeding disrupts microbial communities, potentially leading to dysbiosis, but those studies involved mobile corallivores that move across and among numerous individual hosts. Sedentary parasites like C. violacea that spend long intervals with individual hosts and are dependent on hosts for food and shelter may minimize damage to host microbiomes to assure continued host health and thus exploitation. More mobile consumers that forage across numerous hosts should not experience these constraints. Thus, stability or disruption of microbiomes on attacked corals may vary based on the foraging strategy of coral consumers.

Variable effects of local management on coral defenses against a thermally regulated bleaching pathogen.

Bleaching and disease are decimating coral reefs especially when warming promotes bleaching pathogens, such as Vibrio coralliilyticus. We demonstrate that sterilized washes from three common corals suppress V. coralliilyticus but that this defense is compromised when assays are run at higher temperatures. For a coral within the ecologically critical genus Acropora, inhibition was 75 to 154% greater among colonies from coral-dominated marine protected areas versus adjacent fished areas that were macroalgae-dominated. Acropora microbiomes were more variable within fished areas, suggesting that reef degradation may also perturb coral microbial communities. Defenses of a robust poritid coral and a weedy pocilloporid coral were not affected by reef degradation, and microbiomes were unaltered for these species. For some ecologically critical, but bleaching-susceptible, corals such as Acropora, local management to improve reef state may bolster coral resistance to global change, such as bacteria-induced coral bleaching during warming events.

Biodiversity enhances coral growth, tissue survivorship and suppression of macroalgae.

Coral reefs are declining dramatically and losing species richness, but the impact of declining biodiversity on coral well-being remains inadequately understood. Here, we demonstrate that lower coral species richness alone can suppress the growth and survivorship of multiple species of corals (Porites cylindrica, Pocillopora damicornis and Acropora millepora) under field conditions on a degraded, macroalgae-dominated reef. Our findings highlight the positive role of biodiversity in the function of coral reefs, and suggest that the loss of coral species richness may trigger negative feedback that causes further ecosystem decline.

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.

Intergenerational effects of macroalgae on a reef coral: major declines in larval survival but subtle changes in microbiomes.

Tropical reefs are shifting from coral to macroalgal dominance, with macroalgae suppressing coral recovery, potentially via effects on coral microbiomes. Understanding how macroalgae affect corals and their microbiomes requires comparing algae- versus coral-dominated reefs without confounding aspects of time and geography. We compared survival, settlement, and post-settlement survival of larvae, as well as the microbiomes of larvae and adults, of the Pacific coral Pocillopora damicornis between an Marine Protected Area (MPA) dominated by corals versus an adjacent fished area dominated by macroalgae. Microbiome composition in adult coral, larval coral, and seawater did not differ between the MPA and fished area. However, microbiomes of adult coral were more variable in the fished area and Vibrionaceae bacteria, including strains most closely related to the pathogen Vibrio shilonii, were significantly enriched, but rare, in adult and larval coral from the fished area. Larvae from the macroalgae-dominated area exhibited higher pre-settlement mortality and reduced settlement compared to those from the coral-dominated area. Juveniles planted into a coral-dominated area survived better than those placed into a fished area dominated by macroalgae. Differential survival depended on whether macroalgae were immediately adjacent to juvenile coral rather than on traits of the areas per se. Contrary to our expectations, coral microbiomes were relatively uniform at the community level despite dramatic differences in macroalgal cover between the MPA (~2% cover) and fished (~90%) area. Reducing macroalgae may elicit declines in rare but potentially harmful microbes in coral and their larvae, as well as positive intergenerational effects on offspring survival.

Overlooked coral predators suppress foundation species as reefs degrade.

Loss of larger consumers from stressed ecosystems can lead to trophic release of mid-level consumers that then impact foundation species, suppressing ecosystem function and resilience. For example, in coral reef ecosystems, outbreaks of coral predators like crown-of-thorns sea stars have been associated with fishing pressure and can dramatically impact the composition and persistence of corals. However, the ecological impacts, and consequences for management, of smaller, less obvious corallivores remain inadequately understood. We investigated whether reef state (coral vs. seaweed domination) influenced densities and size frequencies of the corallivorous gastropod Coralliophila violacea on its common host, the coral Porites cylindrica, within three pairs of small Marine Protected Areas (MPAs) and adjacent fished areas in Fiji. C. violacea densities were 5-35 times greater, and their size frequencies more broadly distributed, within seaweed-dominated fished areas than in adjacent MPAs dominated by corals. Tethering snails (4-9 mm in shell height) in place on their coral hosts indicated that suppression of snails in MPAs was due to predation, apparently by fishes. When tethered on the benthos (where they rarely occur), rather than on their host, mortality of larger snails (15.0-25.0 mm in shell height) was high in all areas, primarily due to hermit crabs killing them and occupying their shells. Because C. violacea is a sessile gastropod that feeds affixed to the base of corals and produces minimal visible damage, it has been considered a "prudent feeder" that minimally impacts its host coral. We assessed this over a 24-d feeding period in the field. Feeding by individual C. violacea reduced P. cylindrica growth by ~18-43% depending on snail size. Our findings highlight the considerable, but underappreciated, negative impacts of this common corallivore on degraded reefs. As reefs degrade and corals are lost, remaining corals (often species of Porites) may gain the full attention of elevated densities of coral consumers. This will further damage the remaining foundation species, suppressing the resilience of corals and enhancing the resilience of degraded, seaweed-dominated reefs.

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.

Declines in plant palatability from polar to tropical latitudes depend on herbivore and plant identity.

Long-standing theory predicts that the intensity of consumer-prey interactions declines with increasing latitude, yet for plant-herbivore interactions, latitudinal changes in herbivory rates and plant palatability have received variable support. The topic is of growing interest given that lower-latitude species are moving poleward at an accelerating rate due to climate change, and predicting local interactions will depend partly on whether latitudinal gradients occur in these critical biotic interactions. Here, we assayed the palatability of 50 seaweeds collected from polar (Antarctica), temperate (northeastern Pacific; California), and tropical (central Pacific; Fiji) locations to two herbivores native to the tropical and subtropical Atlantic, the generalist crab Mithraculus sculptus and sea urchin Echinometra lucunter. Red seaweeds (Rhodophyta) of polar and temperate origin were more readily consumed by urchins than were tropical reds. The decline in palatability with decreasing latitude is explained by shifts in tissue organic content along with the quantity and quality of secondary metabolites, degree of calcification or both. We detected no latitudinal shift in palatability of red seaweeds to crabs, nor any latitudinal shifts in palatability of brown seaweeds (Phaeophyta) to either crabs or urchins. Our results suggest that evolutionary pressure from tropical herbivores favored red seaweeds with lower palatability, either through the production of greater levels of chemical defenses, calcification, or both. Moreover, our results tentatively suggest that the "tropicalization" of temperate habitats is facilitated by the migration of tropical herbivores into temperate areas dominated by weakly defended and more nutritious foods, and that the removal of these competing seaweeds may facilitate the invasion of better-defended tropical seaweeds.

Herbivory in the marine realm.

Herbivory occurs when animals consume plants; but the term hides two fundamentally different processes. One relates to the animal's nutrition, the other to the plant's survival and abundance. Both are central to the ecological process called herbivory. Evolutionary innovations in herbivore function have shaped shallow marine ecosystems from kelp forests to coral reefs.

Effects of ocean acidification on the potency of macroalgal allelopathy to a common coral.

Many coral reefs have phase shifted from coral to macroalgal dominance. Ocean acidification (OA) due to elevated CO2 is hypothesised to advantage macroalgae over corals, contributing to these shifts, but the mechanisms affecting coral-macroalgal interactions under OA are unknown. Here, we show that (i) three common macroalgae are more damaging to a common coral when they compete under CO2 concentrations predicted to occur in 2050 and 2100 than under present-day conditions, (ii) that two macroalgae damage corals via allelopathy, and (iii) that one macroalga is allelopathic under conditions of elevated CO2, but not at ambient levels. Lipid-soluble, surface extracts from the macroalga Canistrocarpus (=Dictyota) cervicornis were significantly more damaging to the coral Acropora intermedia growing in the field if these extracts were from thalli grown under elevated vs ambient concentrations of CO2. Extracts from the macroalgae Chlorodesmis fastigiata and Amansia glomerata were not more potent when grown under elevated CO2. Our results demonstrate increasing OA advantages seaweeds over corals, that algal allelopathy can mediate coral-algal interactions, and that OA may enhance the allelopathy of some macroalgae. Other mechanisms also affect coral-macroalgal interactions under OA, and OA further suppresses the resilience of coral reefs suffering blooms of macroalgae.

Size matters: Predator outbreaks threaten foundation species in small Marine Protected Areas.

The unanticipated impacts of consumers in fragmented habitats are frequently a challenge for ecosystem management. On Indo-Pacific coral reefs, crown-of-thorns sea stars (Acanthaster spp.) are coral predators whose outbreaks cause precipitous coral decline. Across large spatial scales, Acanthaster densities are lower in large no-take Marine Protected Areas (MPAs) and reefs subject to limited human exploitation. However, using a combination of observational and manipulative experiments, we found that Acanthaster densities within a network of small, no-take MPAs on reef flats in Fiji were ~2-3.4 times greater inside MPAs than in adjacent fished areas and ~2-2.5 times greater than the upper threshold density indicative of an outbreak. This appeared to result from selective Acanthaster migration to the coral-rich MPAs from fished areas that are coral-poor and dominated by macroalgae. Small MPAs can dramatically increase the cover of foundation species like corals, but may selectively attract coral predators like Acanthaster due to greater food densities within MPAs or because the MPAs are too small to support Acanthaster enemies. As coral cover increases, their chemical and visual cues may concentrate Acanthaster to outbreak densities that cause coral demise, compromising the value of small MPAs. An understanding of predator dynamics as a function of habitat type, size, and fragmentation needs to be incorporated into MPA design and management.