Publications

Ecosystem Recovery Since 1999, broadcasting more than 70 million seeds of the seagrass Zostera marina into coastal lagoons in Virginia has led to the reestablishment of more than 3600 hectares of previously lost seagrass beds. Orth et al. found that seagrass recovery led to rapid increases in the production and diversity of animals, increases in carbon and nitrogen sequestration, decreases in turbidity, and increases in previously depleted bay scallops. This is one of the larger success stories of ecosystem restoration and demonstrates that reversal of ecological collapse is possible when sustained initial efforts lead to positive feedbacks that support ecosystem recovery. Sci. Adv. 10.1126/sciadv.abc6434 (2020).

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.

Strips of the seagrass Thalassia testudinum were used in a field bioassay to assess herbivory on 11 coral reefs scattered throughout the Caribbean. Patterns of herbivory on overfished reefs in Haiti and the United States Virgin Islands were compared to patterns on seven less fished reefs (United States Virgin Islands, Panama, Honduras, Belize, and the Bahamas). On the overfished reefs, the rate of Thalassia removal increased significantly with depth, urchin densities were high, and urchin grazing was equal to, or greater than, fish grazing in shallow (

Inducible defences are widely used for studying phenotypic plasticity, yet frequently we know little about the cues that induce these defences. For aquatic prey, defences are induced by chemical cues from predators (kairomones) and injured prey (alarm cues). Rarely has anyone determined the separate and combined effects of these cues, particularly across phylogenetically diverse prey types. We examined how tadpoles (Hyla versicolor) altered their defences when 10 different prey were either crushed by hand or consumed by predators. Across all prey types, crushing induced only a subset of the defences induced by consumption. Consuming vs. crushing produced additive responses for behaviour but synergistic responses for morphology and growth. Moreover, we discovered the first extensive evidence that prey responses to different alarm cues depends on prey phylogeny. These results suggest that the amount of information available to the prey affects both the quantitative and qualitative nature of the defended phenotype. PMID: 21352454

Pervasive overharvesting of consumers and anthropogenic nutrient loading are changing the strengths of top-down and bottom-up forces in ecosystems worldwide. Thus, identifying the relative and synergistic roles of these forces and how they differ across habitats, ecosystems, or primary-producer types is increasingly important for understanding how communities are structured. We used factorial meta-analysis of 54 field experiments that orthogonally manipulated herbivore pressure and nutrient loading to quantify consumer and nutrient effects on primary producers in benthic marine habitats. Across all experiments and producer types, herbivory and nutrient enrichment both significantly affected primary-producer abundance. They also interacted to create greater nutrient enrichment effects in the absence of herbivores, suggesting that loss of herbivores produces more dramatic effects of nutrient loading. Herbivores consistently had stronger effects than did nutrient enrichment for both tropical macroalgae and seagrasses. The strong effects of herbivory but limited effects of nutrient enrichment on tropical macroalgae suggest that suppression of herbivore populations has played a larger role than eutrophication in driving the phase shift from coral- to macroalgal-dominated reefs in many areas, especially the Caribbean. For temperate macroalgae and benthic microalgae, the effects of top-down and bottom-up forces varied as a function of the inherent productivity of the ecosystem. For these algal groups, nutrient enrichment appeared to have stronger effects in high- vs. low-productivity systems, while herbivores exerted a stronger top-down effect in low-productivity systems. Effects of herbivores vs. nutrients also varied among algal functional groups (crustose algae, upright macroalgae, and filamentous algae), within a functional group between temperate and tropical systems, and according to the metric used to measure producer abundance. These analyses suggest that human alteration of food webs and nutrient availability have significant effects on primary producers but that the effects vary among latitudes and primary producers, and with the inherent productivity of ecosystems.

Because seaweeds uncontrolled by herbivores can overgrow and kill corals, competition can exclude corals from temperate latitudes where herbivores generally fail to control seaweed biomass. In this study, we show that the coral Oculina arbuscula persists on reefs in temperate North Carolina where seaweeds are common by harboring the omnivorous crab Mithrax forceps, which removes seaweeds and invertebrates growing on or near the coral. In the field, corals from which crabs are experimentally removed develop a dense cover of epibionts, exhibiting reduced growth and increased mortality relative to corals with crabs, which remain epibiont-free. This crab is unusual in that it readily consumes all local seaweeds in laboratory choice assays and is not deterred by chemical defenses that suppress feeding by local fishes, sea urchins, and other crabs. This allows Mithrax to defend corals from overgrowth by chemically noxious seaweeds like Dictyota and Sargassum that are avoided by most local herbivores. However, further field manipulations under reduced light conditions demonstrate that the outcome of the crab–coral interaction is context-dependent: crabs only benefit corals in well-lit areas where seaweeds are abundant. Field observations and tethering experiments show that, by living in association with Oculina, Mithrax gains a refuge from predation. Additionally, crabs grow faster when associated with live corals than with structurally equivalent dead corals, apparently because they are able to consume lipid-rich coral mucus. This mucus provides a dietary supplement that may help corals attract and retain low-mobility symbionts such as Mithrax, securing for the coral long-term and predictable protection against competitors. Structurally complex but competitively inferior organisms, like some corals and coralline algae, provide the biogenic habitat complexity upon which many other species depend. Because these sessile organisms may be dependent on symbionts to remove superior competitors, mutualisms can play an important, but currently underappreciated, role in structuring marine communities where biotic interactions are intense. In this study, the mutualism between Oculina and Mithrax promotes the persistence of both species in habitats from which they might otherwise be excluded by competition and predation.

Many tropical seaweeds and benthic invertebrates produce both secondary metabolites and calcium carbonate (CaCO 3 ) particles or spicules that serve as possible defenses against consumers. To evaluate the relative defensive value of CaCO 3 , secondary metabolites, and the potential synergistic or additive effects of the two, we made artificial agar—based “seaweeds” in which we manipulated algal organic content, CaCO 3 , and the secondary metabolites produced by the calcified green seaweeds Rhipocephalus phoenix, Udotea cyathiformis, and Halimeda goreauii, all of which are relatively resistant to herbivores. The effects of these manipulations on herbivore feeding were evaluated using three different types of herbivores, the sea urchin Diadema antillarum, the amphipod Cymadusa filosa, and a mixed—species group of small parrotfishes. Addition of finely powdered CaCO 3 as 69% of food dry mass had no effect on feeding by parrotfishes, deterred feeding by Cymadusa, and deterred Diadema when food organic content was low but not when it was higher. Although calcification of algal tissues has generally been considered a structural defense that hardens seaweed thalli and makes them more resistant to attack, the decreased feeding on CaCO 3 —containing foods in our assays occurred without any measurable alternation of food toughness. At natural concentrations, semipurified secondary metabolites from Rhipocephalus or Udotea deterred feeding by all three herbivores. In most assays, feeding was depressed more by the addition of metabolites from Rhipocephalus or Udotea than by the addition of CaCO 3 even though CaCO 3 was added at 1.3—2.2 times the natural concentration for these plants. In contrast, the major metabolite from Halimeda goreauii, when tested alone, did not affect feeding by any of the herbivores. In two of our nine assays, the synchronous combination of CaCO 3 and secondary metabolites acted synergistically and deterred feeding significantly more than the sum of the effects of each tested separately. Mechanisms producing these synergisms are unknown, but it is possible that calcification could also be acting as a chemical defense by altering gut pH in ways that increase the potency of the secondary metabolites. It is common for chemical, structural, morphological, and nutritional deterrents to co—occur in individual prey species. For some plant—herbivore interactions, the combined effects of these characteristics can be much more than the sum of their separate effects.

Consumer effects on prey are well known for cascading through food webs and producing dramatic top-down effects on community structure and ecosystem function. Bottom-up effects of prey (primary producer) biodiversity are also well known. However, the role of consumer diversity in affecting community structure or ecosystem function is not well understood. Here, we show that herbivore species richness can be critical for maintaining the structure and function of coral reefs. In two experiments over 2 years, we constructed large cages enclosing single herbivore species, equal densities of mixed species of herbivores, or excluding herbivores and assessed effects on both seaweeds and corals. When compared with single-herbivore treatments, mixed-herbivore treatments lowered macroalgal abundance by 54–76%, enhanced cover of crustose coralline algae (preferred recruitment sites for corals) by 52–64%, increased coral cover by 22%, and prevented coral mortality. Complementary feeding by herbivorous fishes drove the herbivore richness effects, because macroalgae were unable to effectively deter fishes with different feeding strategies. Maintaining herbivore species richness appears critical for preserving coral reefs, because complementary feeding by diverse herbivores produces positive, but indirect, effects on corals, the foundation species for the ecosystem.

Climate-driven changes in biotic interactions can profoundly alter ecological communities, particularly when they impact foundation species. In marine systems, changes in herbivory and the consequent loss of dominant habitat forming species can result in dramatic community phase shifts, such as from coral to macroalgal dominance when tropical fish herbivory decreases, and from algal forests to ‘barrens’ when temperate urchin grazing increases. Here, we propose a novel phase-shift away from macroalgal dominance caused by tropical herbivores extending their range into temperate regions. We argue that this phase shift is facilitated by poleward-flowing boundary currents that are creating ocean warming hotspots around the globe, enabling the range expansion of tropical species and increasing their grazing rates in temperate areas. Overgrazing of temperate macroalgae by tropical herbivorous fishes has already occurred in Japan and the Mediterranean. Emerging evidence suggests similar phenomena are occurring in other temperate regions, with increasing occurrence of tropical fishes on temperate reefs.

Previous investigations, focused primarily on vertebrates, have noted substantial losses of eggs and embryos to predators and questioned why selection has not more commonly resulted in the evolution of chemically defended eggs or embryos. Hypotheses regarding the apparent rarity of such defenses have emphasized the potential incompatibility of actively developing tissues and toxic metabolites. Alternatively, this apparent pattern could be an artifact of our greater knowledge of vertebrates, which in general show few tendencies for synthesizing defensive metabolites in either juvenile or adult stages. In this study, we investigated adult and larval chemical defenses of a group of benthic marine invertebrates, the ascidians, in which the adults are often chemically rich, and we contrast our findings with what is known about chemical defenses of eggs and embryos from terrestrial and aquatic organisms. Our findings suggest that there is no fundamental incompatibility of rapidly developing juvenile tissues and bioactive metabolites, and that chemically defended eggs and larval stages may be common among some taxonomic groups. Ascidians are benthic invertebrates that often lack apparent physical defenses against predation, yet are common on coral reefs where predation by fishes is intense. In contrast to most co—occurring invertebrates, many ascidians also release large, conspicuous larvae during daylight hours when exposure to fish predation would be highest. Thus selection by predators might favor the evolution of distasteful larvae. In situ observations indicate that many conspicuous ascidian larvae are distasteful to potential consumers. We investigated the ability of secondary metabolites produced by taxonomically diverse ascidians from geographically distant locales to deter predation on both adults and larvae. Larvae from the Caribbean ascidian Trididemnum solidum were distasteful to reef fishes, and when organic extracts of individual larvae were transferred onto eyes of freeze—dried krill (a good larval mimic in terms of size and color), these eyes were rejected by fishes while control eyes (solvent only) were readily eaten. Larvae of the Indo—Pacific ascidian Sigillina cf. signifera were also distasteful to coral—reef fishes and contained the unpalatable bipyrrole alkaloid tambjamine C. When added to artificial foods at or below their natural mean concentrations and offered to consumers in field and laboratory feeding assays, the secondary metabolites produced by Trididemnum solidum (Caribbean Sea), Sigillina cf. signifera (Indo—Pacific), and Polyandrocarpa sp. (Gulf of California) significantly deterred feeding by co—occurring fishes and invertebrates. Secondary metabolites produced by Trididemnum cf. cyanophorum from the Caribbean Sea, Lissoclinum patella from the Indo—Pacific, and Aplidium californicum from the temperate Pacific, and the small stellate spicules common to many tropical didemnid ascidians did not significantly affect fish feeding. High—pressure liquid chromatography (HPLC) analyses of six didemnin cyclic peptides in individual colonies of Trididemnum solidum from one patch reef at Little San Salvador, Bahamas found large inter—colony differences in their concentrations. The mean concentration of didemnin B was more than double the concentration needed to significantly deter fish feeding in our field assays, and feeding tests with nordidemnin B showed that it deterred fish feeding across the entire range of natural concentrations. HPLC analysis of the extract from a combined collection of T. solidum larvae found adequate concentrations of didemnin B and nordidemnin B to account for their rejection by foraging fishes. We demonstrate that taxonomically diverse ascidians from habitats characterized by intense predation pressure produce secondary metabolites that significantly reduce predation on both adults and larvae, and suggest that this defensive chemistry may be crucial in allowing the release of large, well—provisioned larvae during daylight periods when larvae have the greatest probability of using photic cues to select physically appropriate settlement sites. Production of defensive secondary metabolites appears widespread among certain groups of ascidians, some of which are also known to concentrate acid and heavy metals as additional defensive strategies.