Improving coral cover using an integrated pest management framework.

Integrated pest management (IPM) leverages our understanding of ecological interactions to mitigate the impact of pest species on economically and/or ecologically important assets. It has primarily been applied in terrestrial settings (e.g., agriculture), but has rarely been attempted for marine ecosystems. The crown-of-thorns starfish (CoTS), Acanthaster spp., is a voracious coral predator throughout the Indo-Pacific where it undergoes large population increases (irruptions), termed outbreaks. During outbreaks CoTS act as a pest species and can result in substantial coral loss. Contemporary management of CoTS on the Great Barrier Reef (GBR) adopts facets of the IPM paradigm to manage these outbreaks through strategic use of direct manual control (culling) of individuals in response to ecologically based target thresholds. There has, however, been limited quantitative analysis of how to optimize the implementation of such thresholds. Here we use a multispecies modeling approach to assess the performance of alternative CoTS management scenarios for improving coral cover trajectories. The scenarios examined varied in terms of their ecological threshold target, the sensitivity of the threshold, and the level of management resourcing. Our approach illustrates how to quantify multidimensional trade-offs in resourcing constraints, concurrent CoTS and coral population dynamics, the stringency of target thresholds, and the geographical scale of management outcomes (number of sites). We found strategies with low target density thresholds for CoTS (≤0.03 CoTS min-1 ) could act as "Effort Sinks" and limit the number of sites that could be effectively controlled, particularly under CoTS population outbreaks. This was because a handful of sites took longer to control, which meant other sites were not controlled. Higher density thresholds (e.g., 0.04-0.08 CoTS min-1 ), tuned to levels of coral cover, diluted resources among sites but were more robust to resourcing constraints and pest population dynamics. Our study highlights trade-off decisions when using an IPM framework and informs the implementation of threshold-based strategies on the GBR.

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.

Effects of predation and nutrient enrichment on the success and microbiome of a foundational coral.

By inflicting damage to prey tissues, consumer species may increase stress in prey hosts and reduce overall fitness (i.e., primary effects, such as growth or reproduction) or cause secondary effects by affecting prey interactions with other species such as microbes. However, little is known about how abiotic conditions affect the outcomes of these biotic interactions. In coral reef communities, both nutrient enrichment and predation have been linked to reduced fitness and disease facilitation in corals, yet no study to date has tested their combined effects on corals or their associated microbial communities (i.e., microbiomes). Here, we assess the effects of grazing by a prevalent coral predator (the short coral snail, Coralliophila abbreviata) and nutrient enrichment on staghorn coral, Acropora cervicornis, and its microbiomes using a factorial experiment and high-throughput DNA sequencing. We found that predation, but not nutrients, significantly reduced coral growth and increased mortality, tissue loss, and turf algae colonization. Partial predation and nutrient enrichment both independently altered coral microbiomes such that one bacterial genus came to dominate the microbial community. Nutrient-enriched corals were associated with significant increases in Rickettsia-like organisms, which are currently one of several microbial groups being investigated as a disease agent in this coral species. However, we found no effects of nutrient enrichment on coral health, disease, or their predators. This research suggests that in the several months following coral transplantation (i.e., restoration) or disturbance (i.e., recovery), Caribbean acroporid corals appear to be highly susceptible to negative effects caused by predators, but not or not yet susceptible to nutrient enrichment despite changes to their microbial communities.

Feeding biology of crown-of-thorns seastars across sites differing in Acropora availability.

Crown-of-thorns seastars (COTS, Acanthaster spp.) are a major contributor to coral mortality across the Indo-Pacific and can cause extensive reef degradation. The diet preferences of COTS can influence coral community structure by predation on fast-growing genera such as Acropora and avoidance of rare coral genera. In non-outbreaking populations, this preference can increase species diversity. The feeding biology of Acanthaster cf. solaris was compared at two sites (Shark Alley and Second Lagoon) on One Tree Island reef, located in the southern Great Barrier Reef, to determine whether the availability of Acropora influences differences in COTS movement, feeding preference and feeding rates within the same reef system. Acanthaster cf. solaris were tracked daily for five days across both sites, with measurements of movement, feeding scars and coral composition recorded over this time. While Shark Alley and Second Lagoon have similar live coral cover (40 and 44 % respectively), Shark Alley has significantly lower Acropora availability than Second Lagoon (2 vs 32 %). The feeding rate of COTS was significantly different between Shark Alley and Second Lagoon (259.8 and 733.8 cm2 of coral per day, respectively), but did not differ between seastar size (25-40 cm and >40 cm). Acanthaster cf. solaris showed preference for Pocillopora, Seriatopora, Acropora and Isopora and an avoidance of Porites at both sites. The results suggest that for coral reef sites where Acropora is not dominant, COTS outbreaks may be less likely to initiate, with comparatively low feeding rates found in comparison to coral reefs where Acropora is dominant.

Crown-of-thorns seastar (Acanthaster spp.) feeding ecology across species and regions.

The coral predators, crown-of-thorns starfish (COTS, Acanthaster spp.) remain a major cause of extensive and widespread coral loss in Indo-Pacific coral reefs. With increased phylogenetic understanding of these seastars, at least five species appear to be present across different regions. We compare the feeding ecology of these species. Where acroporid corals are prevalent, Acanthaster spp. often exhibit a preference for these corals, with Porites being least preferred, as seen in most species including Acanthaster planci in the northern Indian Ocean and Acanthaster cf. solaris in the west Pacific. In the eastern Pacific, where Acropora is largely absent, Acanthaster cf. ellisii prey on a range of coral species, including Porites. Coral predation by COTS is influenced by several factors including food availability, coral nutritional value, protective crustaceans and coral defenses, with differences in feeding ecology and behaviour emerging across the different COTS species. Feeding behaviour of COTS can act to increase coral species richness by reducing the dominance of fast-growing species. In outbreaking populations, COTS impacts reef systems by reducing live coral cover, eroding reef complexity and causing shifts in reef trophic structure. Where data are available, we synthesise and contrast the feeding preferences and foraging behaviour of Acanthaster species, and their impact on coral assemblages across the different species and regions. For areas where focal predation on Acropora occurs, also the fastest growing coral with the greatest recovery potential following mass mortality events, the combination of climate change and COTS outbreaks presents an imminent threat to coral reefs. This is exacerbated by the dietary flexibility of Acanthaster species. The impacts of heatwaves, COTS and other stressors are creating a negative feedback loop accelerating coral reef decline.

Fish predation on corals promotes the dispersal of coral symbionts.

BACKGROUND: The microbiomes of foundation (habitat-forming) species such as corals and sponges underpin the biodiversity, productivity, and stability of ecosystems. Consumers shape communities of foundation species through trophic interactions, but the role of consumers in dispersing the microbiomes of such species is rarely examined. For example, stony corals rely on a nutritional symbiosis with single-celled endosymbiotic dinoflagellates (family Symbiodiniaceae) to construct reefs. Most corals acquire Symbiodiniaceae from the environment, but the processes that make Symbiodiniaceae available for uptake are not resolved. Here, we provide the first comprehensive, reef-scale demonstration that predation by diverse coral-eating (corallivorous) fish species promotes the dispersal of Symbiodiniaceae, based on symbiont cell densities and community compositions from the feces of four obligate corallivores, three facultative corallivores, two grazer/detritivores as well as samples of reef sediment and water. RESULTS: Obligate corallivore feces are environmental hotspots of Symbiodiniaceae cells: live symbiont cell concentrations in such feces are 5-7 orders of magnitude higher than sediment and water environmental reservoirs. Symbiodiniaceae community compositions in the feces of obligate corallivores are similar to those in two locally abundant coral genera (Pocillopora and Porites), but differ from Symbiodiniaceae communities in the feces of facultative corallivores and grazer/detritivores as well as sediment and water. Combining our data on live Symbiodiniaceae cell densities in feces with in situ observations of fish, we estimate that some obligate corallivorous fish species release over 100 million Symbiodiniaceae cells per 100 m2 of reef per day. Released corallivore feces came in direct contact with coral colonies in the fore reef zone following 91% of observed egestion events, providing a potential mechanism for the transfer of live Symbiodiniaceae cells among coral colonies. CONCLUSIONS: Taken together, our findings show that fish predation on corals may support the maintenance of coral cover on reefs in an unexpected way: through the dispersal of beneficial coral symbionts in corallivore feces. Few studies examine the processes that make symbionts available to foundation species, or how environmental reservoirs of such symbionts are replenished. This work sets the stage for parallel studies of consumer-mediated microbiome dispersal and assembly in other sessile, habitat-forming species.

Phestilla subodiosus sp. nov. (Nudibranchia, Trinchesiidae), a corallivorous pest species in the aquarium trade.

Phestilla subodiosus sp. nov. (Nudibranchia: Trinchesiidae) is a novel species that feeds on corals in the genus Montipora (Scleractinia: Acroporidae) which are economically important in the aquarium industry. Nuclear-encoded H3, 28SC1-C2, and mitochondrial-encoded COI and 16S markers were sequenced. Phylogenetic analysis, Automatic Barcode Gap Discovery (ABGD), morphological data, and feeding specialization all support the designation of Phestilla subodiosus sp. nov. as a distinct species. Although new to science, Phestilla subodiosus sp. nov. had been extensively reported by aquarium hobbyists as a prolific pest over the past two decades. The species fell into a well-studied genus, which could facilitate research into its control in reef aquaria. Our phylogenetic analysis also revealed Tenellia chaetopterana formed a well-supported clade with Phestilla. Based upon a literature review, its original morphological description, and our phylogenetic hypothesis, we reclassified this species as Phestilla chaetopterana comb. nov.

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.

Intermediate host switches drive diversification among the largest trematode family: evidence from the Polypipapiliotrematinae n. subf. (Opecoelidae), parasites transmitted to butterflyfishes via predation of coral polyps.

Podocotyloides stenometra Pritchard, 1966 (Digenea: Opecoelidae) is the only trematode known to infect anthozoan corals. It causes disease in coral polyps of the genus Porites Link (Scleractinia: Poritidae) and its life-cycle depends on ingestion of these polyps by butterflyfishes (Perciformes: Chaetodontidae). This species has been reported throughout the Indo-Pacific, from the Seychelles to the Galápagos, but no study has investigated whether multiple species are involved. Here, we recollect P. stenometra from its type-host and type-locality, in Hawaiian waters, and describe four new species from examination of 768 butterflyfishes from French Polynesia. On the basis of morphology, phylogeny and life-history, we propose Polypipapiliotrema Martin, Cutmore & Cribb n. gen. and the Polypipapiliotrematinae Martin, Cutmore & Cribb n. subf., for P. stenometra (Pritchard) n. comb., P. citerovarium Martin, Cutmore & Cribb n. sp., P. hadrometra Martin, Cutmore & Cribb n. sp., P. heniochi Martin, Cutmore & Cribb n. sp., and P. ovatheculum Martin, Cutmore & Cribb n. sp. Given the diversity uncovered here and the ubiquity, abundance and diversity of butterflyfishes on coral reefs, we predict that Polypipapiliotrema will prove to comprise a rich complex of species causing disease in corals across the Indo-Pacific. The unique life-cycle of these taxa is consistent with phylogenetic distinction of the group and provides evidence for a broader basis of diversification among the family. We argue that life-cycle specialisation, in terms of adoption of disparate second intermediate host groups, has been a key driver of the diversification and richness of the Opecoelidae, the largest of all trematode families and the group most frequently encountered in coral reef fishes.

Enhanced susceptibility to predation in corals of compromised condition.

The marine gastropod, Coralliophila abbreviata, is an obligate corallivore that causes substantial mortality in Caribbean Acropora spp. Considering the imperiled status of Acropora cervicornis and A. palmata, a better understanding of ecological interactions resulting in tissue loss may enable more effective conservation strategies. We examined differences in susceptibility of A. cervicornis to C. abbreviata predation based on coral tissue condition. Coral tissue condition was a strong determinant of snail prey choice, with snails preferring A. cervicornis fragments that were diseased or mechanically damaged over healthy fragments. In addition, snails always chose fragments undergoing active predation by another snail, while showing no preference for a non-feeding snail when compared with an undisturbed prey fragment. These results indicate that the condition of A. cervicornis prey influenced foraging behavior of C. abbreviata, creating a potential feedback that may exacerbate damage from predation in coral populations compromised by other types of disturbance.

Complex interactions in the control of coral zonation on a Caribbean reef flat.

This study uses short-term assays and long-term transplant experiments to document the potential importance of fish predation and herbivory to the distribution and abundance of reef-building corals in a Caribbean back-reef system. Experimental manipulations of fish access reveal that the zonal patterns of the two reef-building corals Porites astreoides and P. porites f. furcata, dominant on shallow back-reef habitats, are strongly associated with the feeding intensity of parrotfishes. Differential palatability of the two corals to parrotfishes, the proximity of protective cover for large grazers and the availability of small refugia to harbor a cryptic grazer fauna are suggested as major features contributing to the observed patterns. A model predicting the interactions of various algivore/corallivore guilds on the relative dominance of Porites and algal populations is presented.

Abundance, diversity, and feeding behavior of coral reef butterflyfishes at Lord Howe Island.

Endemic species are assumed to have a high risk of extinction because their restricted geographic range is often associated with low abundance and high ecological specialization. This study examines the abundance of Chaetodon butterflyfishes at Lord Howe Island in the south-west Pacific, and compares interspecific differences in local abundance to the feeding behavior and geographic range of these species. Contrary to expected correlations between abundance and geographic range, the single most abundant species of butterflyfish was Chaetodon tricinctus, which is endemic to Lord Howe Island and adjacent reefs; densities of C. tricinctus (14.1 ± 2.1 SE fish per 200m(2)) were >3 times higher than the next most abundant butterflyfish (Chaetodon melannotus), and even more abundant than many other geographically widespread species. Dietary breadth for the five dominant butterflyfishes at Lord Howe Island was weakly and generally negative correlated with abundance. The endemic C. tricinctus was a distinct outlier in this relationship, though our extensive feeding observations suggest some issues with the measurements of dietary breadth for this species. Field observations revealed that all bites taken on benthic substrates by C. tricinctus were from scleractinian corals, but adults rarely, if ever, took bites from the benthos, suggesting that they may be feeding nocturnally and/or using mid-water prey, such as plankton. Alternatively, the energetic demands of C. tricinctus may be fundamentally different to other coral-feeding butterflyfishes. Neither dietary specialization nor geographic range accounts for interspecific variation in abundance of coral reef butterflyfishes at Lord Howe Island, while much more work on the foraging behavior and population dynamics of C. tricinctus will be required to understand its' abundance at this location.