Notes: Mutualisms occur when interactions between species produce reciprocal benefits. However, the outcome of these interactions frequently shifts from positive, to neutral, to negative, depending on the environmental and community context, and indirect effects commonly produce unexpected mutualisms that have community-wide consequences. The dynamic, and context dependent, nature of mutualisms can transform consumers, competitors, and parasites into mutualists, even while they consume, compete with, or parasitize their partner species. These dynamic, and often diffuse, mutualisms strongly affect community organization and ecosystem processes, but the historic focus on pairwise interactions decoupled from their more complex community context has obscured their importance. In aquatic systems, mutualisms commonly support ecosystem-defining foundation species, underlie energy and nutrient dynamics within and between ecosystems, and provide mechanisms by which species can rapidly adjust to ecological variance. Mutualism is as important as competition, predation, and physical disturbance in determining community structure, and its impact needs to be adequately incorporated into community theory.

Notes: Abstract The potential for spatial associations between palatable and unpalatable plant species to reduce herbivore pressure on the palatable species has been described as associational resistance, associational refuge or associational defense for numerous terrestrial and marine communities. One of the closest associations between species-epibiosis-has not been thoroughly investigated in this regard. In this study we evaluated how different associations between host seaweeds and epibiotic plants and animals influenced the movement of an omnivorous sea urchin (Arbacia punctulata) to the host and subsequent feeding on the host. A. punctulata showed clear preferences when given pairwise choices between 12 prey species (3 animals, 9 algae). These preferences were consistent and allowed us to rank the six epibiont species and six host species linearly from least to most preferred by A. punculata. Most host-epibiont associations dramatically changed urchin preference, increasing or decreasing urchin grazing on fouled hosts as compared to clean conspecifics. Herbivory on the host increased when the epibiont was more preferred, and decreased when it was less preferred than the unfouled host alga. Taking the host species as a point of reference, we classified epibiosis-caused decrease in herbivory as associational resistance, while epibiont-caused increases in herbivory were defined as shared doom. These epibiont-host-herbivore interactions could select for hosts that facilitate the growth of certain low preference epibionts on their surfaces in situations where the resulting decreases in herbivory would offset the various negative effects of being fouled. In contrast, in situations where herbivores are common, the negative effects of being fouled by palatable epibionts may be much greater than is generally assumed. In our assays, unpalatable hosts fouled by palatable epibionts became much more attractive to urchins and rose several ranks on the urchins' preference hierarchy.

Notes: Abstract On Caribbean coral reefs, high rates of grazing by herbivorous fishes are thought to benefit corals because fishes consume competing seaweeds. We conducted field experiments in the Florida Keys, USA, to examine the effects of grazing fishes on coral/seaweed competition. Initially, fragments of Porites divaracata from an inshore habitat were transplanted into full-cage, half-cage, and no-cage treatments on a fore-reef. Within 48 h, 56% of the unprotected corals in half-cage and no-cage treatments (62 of 111) were completely consumed. Stoplight parrotfish (Sparisoma viride) were the major coral predators, with redband parrotfish (S. aurofrenatum) also commonly attacking this coral. Next, we transplanted fragments of P. porites collected from the fore-reef habitat where our caging experiments were being conducted into the three cage treatments, half in the presence of transplanted seaweeds, and half onto initially clean substrates. The corals were allowed to grow in these conditions, with concurrent development of competing seaweeds, for 14 weeks. Although seaweed cover and biomass were both significantly greater in the full-cage treatment, coral growth did not differ significantly between cage treatments even though corals placed with pre-planted seaweeds grew significantly less than corals placed on initially clean substrate. This surprising result occurred because parrotfishes not only grazed algae from accessible treatments, but also fed directly on our coral transplants. Parrotfish feeding scars were significantly more abundant on P. porites from the half and no-cage treatments than on corals in the full cages. On this Florida reef, direct fish predation on some coral species (P. divaracata) can exclude them from fore-reef areas, as has previously been shown for certain seaweeds and sponges. For other corals that live on the fore-reef (P. porites), the benefits of fishes removing seaweeds can be counterbalanced by the detrimental effects of fishes directly consuming corals.

Notes: Abstract Studies of factors affecting host plant specialization by herbivores commonly highlight the value of the plant as both food and habitat, but often cannot distinguish the relative importance of these plant traits. A different approach is to study non-herbivorous animals that specialize on particular plants but do not feed on tissue from these plants. Such animals will not be affected directly by the nutritional, chemical, or morphological traits that determine the value of the plant as a food. This study reports on a filter-feeding amphipod, Ericthoniusbrasiliensis, that lives in domiciles it constructs by curling terminal segments of the green, calcified, and chemically defended seaweed Halimedatuna. We examined the temporal (1850s–1990s) and spatial (Caribbean, Mediterranean, and Pacific regions) scale of the association, the factors that may select for specialization on H. tuna, and the effect of the amphipod on growth of its host. Sampling along 125 km of coral reefs in the Florida Keys (USA) indicated that almost all populations of H. tuna had been colonized by this amphipod. Infested plants occurred on nine of ten reefs that supported H. tuna populations, with between 8 and 75% of the plants on those reefs colonized by the amphipod. For infested plants, 2–23% of all segments on each plant had been curled by the amphipod. Common co-occurring congeners of H. tuna (H. opuntia and H. goreaui) were never used for domicile construction. A survey of 1498 Halimeda specimens collected during the last 140 years and archived in the U.S. National Museum of Natural History (Smithsonian Institution, Washington, D.C.) indicated that the association has existed for 〉100 years and occurs throughout the Caribbean region, never in the Indo-Pacific or Mediterranean, and only on H. tuna. Predation by fishes could select for amphipod specialization on H. tuna. Laboratory experiments demonstrated that amphipods inhabiting curled segments of H. tuna were relatively immune from fish predation while those on the exterior surface of the plant or in open water were rapidly eaten. Segments of H. tuna are large enough to provide full protection from predators, while those of the co-occurring congeners H. goreaui and H. opuntia are of a size that may provide only partial protection. Experimental addition of E. brasiliensis to H. tuna plants in the field significantly decreased segment accumulation on infested relative to uninfested control plants. Whether this negative effect was a direct or indirect consequence of amphipod occupancy is unclear. Rolling plant portions into domiciles could directly decrease host growth by increasing shading and decreasing exposure of plant surface area to water column nutrient flux. Amphipod occupancy could indirectly slow net host growth if fishes selectively feed on plant sections occupied by amphipods. Underwater video showed that herbivorous fishes did not graze infested plants more than uninfested plants, but small predatory fishes did prefer feeding from infested plants. These non-herbivorous fishes may slow host growth by damaging the terminal meristematic tissues of plants during attacks on amphipods. This study demonstrates that habitat specialists can negatively impact hosts without consuming them and that specialization on a plant can occur due to its habitat value alone (as opposed to its value as a food).

Notes: Abstract Within-plant variation in the concentration of secondary metabolites, nutritive value, toughness, and susceptibility to herbivory was assessed for the brown alga Dictyota ciliolata. When young apices and older tissue from the same plant were offered in equal abundance to the herbivorous amphipod Ampithoe longimana and the sea urchin Arbacia punctulata, young apices were consumed about 2 times more than older tissue. Compared to young apices, the less preferred older tissue had a less palatable lipophilic extract, significantly higher concentrations of two secondary metabolites (another secondary metabolite did not differ significantly), 33% more soluble protein, and was 233% tougher. Higher levels of chemical defenses in older tissues, and not tissue toughness or nutritive value, appear to be responsible for the preference of Ampithoe longimana for young apices. The pattern of lower levels of chemical defenses in young than older tissues of D. ciliolata is the opposite of the pattern observed in coenocytic seaweeds and most vascular terrestrial and marine plants, all of which have translocation systems for moving materials among plant portions. Unlike these other plants, which preferentially allocate chemical defenses to young tissues, D. ciliolata cannot readily translocate secondary metabolites. The growth-differentiation balance hypothesis suggests that actively dividing and expanding cells are less able to produce secondary metabolites. This hypothesis may help explain why older tissues are better defended than young, rapidly growing apices.

Notes: Abstract Because encrusting coralline algae rely on herbivory or low light levels to prevent being overgrown by competitively superior fleshy algae, corallines are relatively rare in shallow areas with low rates of herbivory. In contrast to this general trend, the branching coralline alga Neogoniolithon strictum occurs primarily in shallow seagrass beds and along the margins of shallow reef flats where herbivory on macrophytes is low. This alga apparently persists in these habitats by providing refuge to the herbivorous crab Mithrax sculptus at mean densities of 1 crab per 75 g of algal wet mass. When crabs were removed from some host corallines, hosts without crabs supported 9 times the epiphytic growth of hosts with crabs after only 30 days. Crabs without access to a coralline alga were rapidly consumed by reef fishes, while most of those tethered near a host alga survived. These results suggest that the crabs clean their algal host of fouling seaweeds and associate with the host to minimize predation. However, to effectively clean the host, the crab must consume the wide array of macroalgae that commonly co-occur with coralline algae in these habitats, including chemically defended species in the genera Halimeda, Dictyota, and Laurencia. Crabs did readily consume these seaweeds, which were avoided by, and are chemically defended from, herbivorous fishes. Even though crabs readily consumed both Halimeda and Dictyota in whole-plant feeding assays, chemical extracts from these species significantly reduced crab feeding, suggesting that factors other than secondary chemistry (e.g., food value, protein, energy content), may determine whole-plant palatability. Having the ability to use a wide variety of foods, and choosing the most profitable rather than the least defended foods, would diminish foraging time, increase site fidelity, and allow the crab to function mutualistically with the host alga. Despite the obvious benefit of associating with N. strictum, M. sculptus did not prefer it over other habitats offering a structurally similar refuge, suggesting that these crabs are not N. strictum specialists, but rather occupy multiple habitats that provide protection from predators. Structurally complex organisms like N. strictum may commonly suppress competitors by harboring protective symbionts like M. sculptus. It is possible that diffuse coevolution has occurred between these two groups; however, this seems unlikely because both herbivore and host appear to respond most strongly to selective pressures from predators and competitors outside this association.

Notes: Abstract We tested whether grazing by the specialist beetle Galerucella nymphaeae (Coleoptera: Chrysomelidae) induced resistance to herbivory in the water lily Nuphar luteum macrophyllum (Nymphaeaceae) using both the specialist beetle and the generalist crayfish Procambarus clarkii (Decapoda: Cambaridae). For 2 months, we allowed natural densities of beetles to develop on control plants of Nuphar, while removing beetles every 2–3 days from adjacent plants that were paired by location within our field site. By the end of the 2-month manipulation, beetle grazing had damaged twice as much leaf surface on control plants as on removal plants (30.6% vs. 14.2%, respectively). We then offered tissues from control and removal plants to adult and larval beetles and to crayfish in laboratory assays. Increased levels of previous attack by the specialist beetle either did not affect or increased water lily attractiveness to beetles, but significantly decreased attractiveness to the generalist crayfish. Beetle larvae did not feed preferentially on control vs. removal Nuphar in assays using either immature, undamaged leaves that had not yet reached the pond surface or intermediate aged leaves that had reached the surface and experienced some beetle grazing. Adult beetles consumed significantly more immature leaf tissue from the heavily grazed controls than from the less grazed removal plants but did not discriminate between control and removal leaves of intermediate age in either feeding or oviposition preference. In contrast, generalist crayfish consumed significantly more plant tissue from the less grazed treatment than from the more heavily grazed controls. Crude chemical extracts from Nuphar strongly deterred crayfish feeding, but neither phenolic content, protein content, nor differential effects of crude extracts from control vs. removal plants explained crayfish feeding on control versus removal leaves. Our assays suggest that induced resistance to crayfish may be chemically mediated, but the particular mechanisms producing this response remain unclear. Responses may be due to defensive metabolites that degrade rapidly following extraction.

Notes: Summary When the common sea urchin Diadema antillarum was removed from a 50 m strip of reef in St. Thomas, US Virgin Islands, cover of upright algae and the grazing rates and densities of herbivorous parrotfish and surgeonfish increased significantly within 11–16 weeks when compared to immediately adjacent control areas. Sixteen months after removal, Diadema had recovered to 70% of original density, abundance of upright algae no longer differed between removal and control areas, and the abundance and grazing activity of herbivorous fish in the removal was approaching equivalence with control areas. On a patch reef in St. Croix that had been cleared of Diadema 10–11 years earlier (Ogden et al. 1973b), urchins had recovered to only 50–60% of original density. This reef still showed significantly higher rates of grazing by fish and a significantly greater density of parrotfish and surgeonfish than a nearby control reef where Diadema densities had not been altered. These results indicate that high Diadema densities (7–12/m2 for this study) may suppress the densities of herbivorous fish on Caribbean reefs.

Notes: Summary Tropical seaweeds in the genus Halimeda reduce losses to grazing by capitalizing on diel patterns of herbivore activity. These seaweeds produce new, more herbivoresusceptible growth at night when herbivorous reef fishes are inactive. Plant portions more than 48 h old are low in food value, well defended morphologically (calcified and high in ash content), and relatively resistant to herbivory. Younger plant portions represent 3–4.5 times the food value (nitrogen or organic content) of older portions but are only moderately more susceptible to herbivores due to their high concentrations of the terpenoid feeding deterrents halimedatrial and halimedatetraacetate. Halimedatrial significantly deters grazing by both parrotfishes (Scaridae) and surgeonfishes (Acanthuridae) and occurs in high concentrations (2–4.5% of plant ash-free dry mass) in plant portions that are 4–12 h old, intermediate concentrations (0.3–2.3%) in portions that are 16–26 h old, and low concentrations (0.3%) in older plant portions. The related compound halimedatetraacetate is absent from the youngest plant portions, shows a rapid increase in concentration (from 0 to 1%) in plant material that is approximately 16 h old, and then rapidly declines to low levels (0.1 to 0.2%) in older plant portions. Thus, newly produced tissues are nutritionally valuable but contain high concentrations of defensive chemicals. As these tissues age, morphological defenses increase, the tissue becomes less valuable as a food for herbivores, and chemical defenses decrease. Additionally, new growth of Halimeda remains unpigmented until just before sunrise. Thus, the valuable, nitrogen-containing molecules associated with photosynthesis are not placed in the new, and more herbivore susceptible, growth until lights is available and they can start producing income for the plant. Experiments in a coral-reef microcosm, where diel patterns of light and water chemistry could be altered, indicated that Halimeda's growth pattern is cued by the timing of light-dark cycles rather than by co-occurring diel changes in water chemistry. Although the growth patterns of Halimeda seem unusual, similar patterns appear to occur in numerous other seaweeds and in microalgae such as diatoms and dinoflagellates.