Mark E. Hay

Marine chemical ecology: what's known and what's next?

In this review, I summarize recent developments in marine chemical ecology and suggest additional studies that should be especially productive. Direct tests in both the field and laboratory show that secondary metabolites commonly function as defenses against consumers. However, some metabolites also diminish fouling, inhibit competitors or microbial pathogens, and serve as gamete attractants; these alternative functions are less thoroughly investigated. We know little about how consumers perceive secondary metabolites or how ecologically realistic doses of defensive metabolites affect consumer physiology or fitness, as opposed to feeding behavior. Secondary metabolites have direct consequences, but they do not act in isolation from other prey characteristics or from the physical and biological environment in which organisms interact with their natural enemies. This mandates that marine chemical ecology be better integrated into a broader and more complex framework that includes aspects of physiological, population, community, and even ecosystem ecology. Recent advances in this area involve assessing how chemically mediated interactions are affected by physical factors such as flow, desiccation, UV radiation, and nutrient availability, or by biological forces such as the palatability or defenses of neighbors, fouling organisms, or microbial symbionts. Chemical defenses can vary dramatically among geographic regions, habitats, individuals within a local habitat, and within different portions of the same individual. Factors affecting this variance are poorly known, but include physical stresses and induction due to previous attack. Studies are needed to assess which consumers induce prey defenses, how responses vary in environments with differing physical characteristics, and whether the ‘induced’ responses are a direct response to consumer attack or are a defense against microbial pathogens invading via feeding wounds. Although relatively unstudied, ontogenetic shifts in concentrations and types of defenses occur in marine species, and patterns of larval chemical defenses appear to provide insights into the evolution of complex life cycles and of differing modes of development among marine invertebrates. The chemical ecology of marine microbes is vastly underappreciated even though microbes produce metabolites that can have devastating indirect effects on non-target organisms (e.g., red tide related fish kills) and significantly affect entire ecosystems. The natural functions of these metabolites are poorly understood, but they appear to deter both consumers and other microbes. Additionally, marine macro-organisms use metabolites from microbial symbionts to deter consumers, subdue prey, and defend their embryos from pathogens. Microbial chemical ecology offers unlimited possibilities for investigators that develop rigorous and more ecologically relevant approaches.

Patterns of Fish and Urchin Grazing on Caribbean Coral Reefs: Are Previous Results Typical?

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 (<10 m deep) habitats. On reefs subject to little fishing pressure, the rate of Thalassia removal decreased with depth, urchin densities were low, and herbivorous fishes were responsible for almost all Thalassia removal. Previous studies assessing the importance of urchin grazing in the Caribbean have been conducted on overfished reefs where urchin densities were unusually high and the density of grazing fish unusually low. It is doubtful that the intensity of urchin—algal and urchin—coral interactions observed on these heavily fished reefs occurs on reefs unaffected by humans.

STRONG IMPACTS OF GRAZING AMPHIPODS ON THE ORGANIZATION OF A BENTHIC COMMUNITY

Large brown seaweeds dominate coastal hard substrata throughout many of the worlds oceans. In coastal North Carolina, USA, this dominance by brown seaweeds is facilitated by omnivorous fishes, which feed both on red and green algae and on herbivorous amphipods that graze brown algae. When fish are removed in the field, brown seaweeds are replaced by red seaweeds, and herbivorous amphipods are more abundant. Using an array of large (;4000 L) outdoor mesocosms, we tested three mechanistic hypotheses for this pattern: fish feeding facilitates brown algal dominance (1) by removing red and green algal competitors, (2) by removing amphipods and reducing their feeding on brown sea- weeds, or (3) through an interaction of these mechanisms. Our experiments revealed strong impacts of both fish and amphipods, and a key role for the interaction, in structuring this community. When both fish and amphipods were removed (the latter with dilute insecticide), space was rapidly dominated and held for 17 weeks by fast-growing, primarily filamentous green algae. In contrast, when either fish, amphipods, or both were present, green algae were cropped to a sparse turf, and space was more rapidly dominated by larger macroalgae. The impacts of amphipods and fish on late-successional macroalgal assemblages were comparable in magnitude, but different in sign: red seaweeds prevailed in the amphipod- dominated treatment, whereas browns dominated in the presence of fish. Laboratory feeding assays and amphipod densities in the tanks suggested that the significant effects of am- phipods were attributable largely, if not exclusively, to the single amphipod species Am- pithoe longimana, which fed heavily on brown macroalgae. Our experimental removal of red and green algae failed to enhance cover of brown algae significantly; however, the latter reached substantially lower cover in the grazer-removal treatment, where green algae were very abundant, than in the fish-only treatment, where green algae were sparse. Thus, our results support the third hypothesis: fish-mediated dominance of brown algae involves both suppression of grazing amphipods and removal of algal competitors. Although collective impacts of fish and amphipods on this benthic community were generally comparable in magnitude, impacts normalized to each grazers aggregate biomass were consistently higher for amphipods than for fish, sometimes by 1-2 orders of magnitude. Thus, the impacts of grazing amphipods (specifically A. longimana) on the benthic community were both strong and disproportionate to their biomass. These experimental results imply that grazing am- phipods, which are ubiquitous in marine vegetation but poorly understood ecologically, may play important roles in the organization of benthic communities, particularly where predation pressure is low.

Herbivore vs. nutrient control of marine primary producers: context-dependent effects.

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.

Chemical defense against different marine herbivores: are amphipods insect equivalents?

The Structurally similar diterpenoid alcohols pachydictyol-A and dictyol-E are produced by the brown seaweed Dictyota dichotoma. This seaweed and several related species that also produce these compounds are known to be relatively low preference foods for tropical fishes and urchins. We evaluated the effect of various concentrations of these compounds on feeding by the three common types of herbivores that co-occur with Dictyota in coastal North Carolina. Fish (Diplodus holbrooki), sea urchins (Arbacia punctulata), and a mixed species group of gammarid amphipods were offered pieces of the palatable seaweed Gracilaria tikvahiae coated with either (1) dictyol-E or pachydictyol-A dissolved in diethyl ether or (2) diethyl ether alone. Dictyol-E significantly reduced consumption by fish and urchins at concentrations of 0.5 and 1.0% of algal dry mass, but had no effect on amphipod grazing. Pachydictyol-A significantly reduced fish grazing at the relatively high concentrations of 1.0 and 1.3% of plant dry mass; at 0.5% it tended to decrease grazing, but the effect was not significant (P = .07). Pachydictyol-A had no effect on urchin grazing and significantly increased amphipod grazing. When Pachydictyol-A was fed to fish as 1.0% of food dry mass, their growth rate was reduced by a significant 48%. In feeding preference experiments with several seaweeds, Dictyota ranks low for fish and urchins but high for amphipods. This is consistent with the hypothesis that the secondary metabolites produced by Dictyota play a major role in determining its susceptibility to herbivores. The ability of amphipods to circumvent the chemical defenses (Dictyota, and the fact that the two species of algae most readily consumed by amphipods (Codium and Dictyota) were the two species least readily consumed by fish, suggest that predation and herbivory by fishes may be major factors selecting for amphipods that can live on, and eat, seaweeds that are unpalatable to fishes. Amphipods that fed on Dictyota did not appear to sequester the Dictyota metabolites; when exposed to fish predation, Dictyota-fed amphipods were eaten as readily as amphipods that had fed on an alga with no defensive chemistry. Tubicolous amphipods and other small marine herbivores that may spend significant portions of their lives on only a few plants my be under very different evolutionary constraints than the larger, more mobile herbivores that commonly moved between many plants. Several characteristics of these smaller, less mobile, and much less studied, marine herbivores suggest that they may be ecologically similar to terrestrial insects and may play a large, but presently unappreciated, role in structuring marine plant communities.

Associational Plant Defenses and the Maintenance of Species Diversity: Turning Competitors Into Accomplices

The palatable plants investigated in this study gained significant protection from herbivores by associating with abundant competitors that were less susceptible to herbivory. When herbivores were excluded, palatable species associated with unpalatable ones grew at only 14%-19% of the rate of palatable plants separated from unpalatable ones. When herbivores were present, however, palatable species appeared to depend completely on unpalatable competitors to provide microsites of reduced herbivory to prevent grazers from causing local extinction of the preferred species. For the species studied here, the cost of being associated with a larger, unpalatable competitor was much less than the cost of increased consumption in the absence of that competitor. Under these conditions, one competitor can have a strong positive effect on another. Associational defenses can provide an unappreciated mechanism for maintaining species richness within communities that are dominated by one or a few major species. In this community, increases in the abundance of common late-successional competitors led to increases, not decreases, in the abundance and number of other species and to retention, not exclusion, of early-successional species.

The Functional Morphology of Turf-Forming Seaweeds: Persistence in Stressful Marine Habitats

Many seaweeds that occur in physically stressful habitats or habitats subject to mod- erate herbivory grow as colonial turfs rather than as spatially separated individuals. The turf growth form is energetically expensive (the net production per gram ash free dry mass of turfs being 33-61% lower than that of individuals), but turfs suffer less physiological damage during desiccating low tides and lose less biomass to herbivores. The upper portions of turf-forming species show significantly greater rates of apparent photosynthesis and dark respiration than do the lower portions. This spatial partitioning of photosynthetic activity decreases the energetic cost of the turf arrangement and may allow basal portions to function as persistent resting stages during periods of adverse conditions when uprights cannot be maintained. Turf-forming species are specialized for areas that are subject to moderate grazing pressure and physical stresses. They are dependent upon these factors to prevent their competitive exclusion by more productive, but less resistant, seaweeds. Damage to apical por- tions causes increased branching that results in a more tightly compacted turf. Algae that regenerate in this way can adjust their growth form in accordance with varying levels of disturbance encountered in different habitats and thus incur the minimal cost consistent with survival in that area. For seaweeds occurring in stressful habitats, selection has favored characteristics that increase persistence in space and time even though these involve considerable losses in competitive ability and productivity.

Can quantity replace quality ? Food choice, compensatory feeding, and fitness of marine mesograzers

Relationships among food choice, compensatory feeding, and the consequences for consumer fitness rarely have been quantified. We created foods of varying nutritional quality and evaluated the consequences of compensatory feeding for three sympatric species of amphipods by analyzing food choices, feeding rates, and long-term effects on fitness. Nutritional quality was manipulated by creating low-quality diets from algae (low in protein, nitrogen, and total organic carbon), high-quality diets from commercial fish food (high in protein, nitrogen, and total organic carbon), and intermediate-quality diets from mixtures of those two foods. When high- and low-quality diets were simultaneously offered, the more mobile, non-tube-building amphipods, Gammarus mucronatus and Elasmopus levis, both fed preferentially on the high-quality diet. The more sedentary, tube-building amphipod Ampithoe longimana did not discriminate between these foods. When confined to a single food type, all three species exhibited compensato...

Food and Shelter as Determinants of Food Choice by an Herbivorous Marine Amphipod

Because food and habitat are closely linked for small herbivores that live on plants, food choice in the field may be constrained by the need to choose plants that provide safe living sites. We investigated the importance of food value and refuge value in determining the plant utilization patterns of the herbivorous marine amphipod Ampithoe longimana. When offered a choice of five common seaweeds, this amphipod fed most readily on Dictyota and Hypnea and less readily on Sargassum, Chondria, and Calonitophyllum. Rates of feeding on the different seaweeds were unrelated to seaweed gross morphology, toughness, nitrogen, or protein content. When cultured on each of these seaweeds in the laboratory, amphipod survivorship was high on Dictyota (82%), intermediate (35 and 18%, respectively) on Sargassum and Hypnea, and low (0%) on the other seaweeds. Survivorship on the different diets was strongly correlated (r = 0.930) with algal protein content; however, neither protein content nor amphipod performance on the different diets was significantly related to feeding rates on those diets. Additionally, amphipods from the three seaweed species that produced some survivors did not differ in growth rate, fecundity, egg size, or age at first ovulation. Variance in survivorship, and related measures, among sibling groups of amphipods suggested that this amphipod population possessed heritable variation for performance on the different seaweed species. In the field, abundance of A. longimana on the different species of algae was more clearly related to the preference of omnivorous fishes for these algae than to feeding rates of the amphipods when given those algae in the laboratory. A. longimana was more abun- dant on Dictyota and Sargassum (both unpalatable to omnivorous fishes), than on Hypnea, Chondria, and Calonitophyllum (all of which are palatable to fishes). During the season when omnivorous fishes were abundant, density of A. longimana increased on Dictyota, which is chemically defended from fishes, but decreased or remained unchanged on the seaweeds that are more palatable to fishes. Competition with other amphipods as a group did not appear to explain the distribution of A. longimana among seaweeds, since there were no negative correlations between A. longimana abundance and total amphipod abun- dance in any month. The lack of any consistent relationship between host-plant use in the field and either feeding preference or diet value, as measured by survivorship and repro- duction, suggests that host-plant use by A. longimana may be strongly constrained by requirements for shelter from predation.

Herbivore species richness and feeding complementarity affect community structure and function on a coral reef

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.