Greg Cronin

Susceptibility to herbivores depends on recent history of both the plant and animal

Physical stress to seaweeds and hunger stress of herbivores can influence the outcome of chemically mediated seaweed-herbivore interactions. The unpalatable brown seaweed Dictyota ciliolata produces the diterpenoid secondary metabolites pachydictyol A, dictyol B acetate, and dictyodial. At natural concentrations, pachydictyol A deterred the sea urchin Arbacia punctulata but did not inhibit feeding by the pinfish Lagodon rhomboides or the amphipod Ampithoe longimana until concentrations were 2.5-5 times natural levels. Dictyol B acetate deterred the urchin, amphipod, and pinfish at, or far below, natural concentrations. Dictyodial was too unstable to assay directly, but indirect experiments suggested that natural concentrations deterred the urchin, but not the pinfish or amphipod. Mild desiccation of D. ciliolata reduced concentrations of the different secondary metab- olites by 7-38% and plants became 2.6-3.4 times more susceptible to urchin and amphipod grazing. The combined concentrations of pachydictyol A and dictyol B acetate found in undesiccated Dictyota ciliolata deterred feeding by urchins, but this deterrent effect was lost at concentrations found in the desiccated plants. Desiccated and undesiccated plants did not differ in nutritive value (as measured by protein and total N content) or toughness. Thus, desiccated plants became more palatable because chemical defenses were lost, not because nutritive value was increased. The stress of near-surface ultraviolet radiation also caused significant physiological changes in Dictyota ciliolata. UV-exposed blades bleached, senesced, and grew 84% less than blades protected from UV radiation. Tissue loss and minimal growth of UV-stressed plants constrained our sample sizes, but the limited assays that could be run suggested that UV stress may lower chemical defenses and increase plant susceptibility to herbivores. Because many previous investigations of herbivore feeding patterns used animals that had been starved for days before an assay, we tested the effects of this commonly used procedure on feeding discrimination. Recently fed urchins always avoided food containing natural concentrations of pachydictyol A during separate feeding trials performed on each of four consecutive days. In contrast, urchins deprived of food for 3 d before this assay did not avoid the treated food on days 1 and 2 of feeding trials, but did avoid it on days 3 and 4 after their hunger was reduced by feeding during days 1 and 2. If we had used only starved urchins (a common procedure in previous investigations), we could have concluded, with apparent justification, that urchins were unaffected by pachydictyol A (if the assays were run for only 1-2 d) or that they needed 2 d of exposure to the compound in order to learn to avoid it. Both of these conclusions would have been incorrect.

Induction of Seaweed Chemical Defenses by Amphipod Grazing

Grazing by the generalist amphipod Ampithoe longimana induced increased concentrations of defensive secondary metabolites in the brown alga Dictyota menstrualis and made the seaweed less susceptible to further attack by the amphipod. Although A. longimana preferentially consumes D. menstrualis, its feeding rates can be reduced sig- nificantly by high concentrations of diterpenoid dictyols produced by the alga. In 1991, D. menstrualis from sites with high numbers of A. longimana had higher levels of grazing scars, higher concentrations of dictyols, and were less palatable to A. longimana than plants from sites with few amphipods. Among-site differences in palatability to amphipods did not correlate with plant differences in protein, nitrogen, or carbon content. Within a site, plants that had apparent amphipod grazing scars were significantly less palatable to A. Iongimana than neighboring undamaged plants. Controlled field experiments manipulating A. longimana densities supported the hypothesis that feeding by this amphipod induced elevated chemical defenses in the alga. Compared to undamaged control plants, amphipod- damaged plants had 19-34% more of three diterpenoid secondary metabolites and were 50% less palatable to amphipods. Soluble protein and thallus toughness were unaffected by amphipod grazing and thus could not have caused the differences in palatability. High- pressure liquid chromatography evaluation of adventitious branches growing from blade margins at sites of amphipod grazing scars showed that these branches had significantly elevated levels of two diterpenoids relative to normal blade apices or middles. Thus, the amphipod-induced resistance to further attack occurs through an increase in chemical de- fenses, and these defenses are, to some extent, localized within the plant thallus. Among- site differences in amphipod densities, grazing scars, seaweed defensive chemistry, and plant palatability that we documented in 1991 varied considerably during 1992 and 1993, suggesting that these interrelationships may be complex. In 1992, A. longimana densities did not differ between sites, and there were no between-site differences in palatability or concentrations of deterrent secondary metabolites. In 1993, however, A. Iongimana densities did differ between sites, but between-site differences were less dramatic than in 1991. Some secondary metabolites were slightly, but significantly, increased at the site with higher densities of A. longimana, but this had no effect on A. longimana feeding. It has been long recognized that marine herbivores are active participants in seaweed- herbivore interactions and can greatly influence the structure of benthic algal communities. Our findings suggest that seaweeds are not passive participants in these interactions, but can actively alter their susceptibility to herbivores in ecological time. Induced responses to herbivory help explain both spatial (i.e., within-thallus, within-site, and among-site) and temporal variation in the chemical defenses of D. menstrualis.

Impact of herbivory on plant standing crop: comparisons among biomes, between vascular and nonvascular plants, and among freshwater herbivore taxa

Two contradictory traditions exist regarding the impact of herbivores on the ecology and evolution of plants. For ecologists studying terrestrial ecosystems, the interaction between plants and their consumers has been a focal point for research in recent decades. Herbivores are widely regarded as an important determinant of plant abundance and species composition and as an important selective force in the evolution of terrestrial plant traits (Rhoades, 1985; Herms, and Mattson, 1992; Rosenthal and Berenbaum, 1992). Similarly, the abundance of many marine plants is often reduced by herbivores, and many seaweed traits are thought to have evolved in response to herbivory (Lubchenco and Gaines, 1981; Gaines and Lubchenco, 1982; Estes and Steinberg, 1988; Hay, 1991). By contrast, for decades the paradigm in limnology has been that live freshwater macrophytes are too tough for the mouthparts of aquatic herbivores, are of low nutritional quality, and are rarely consumed by herbivores (Lodge, 1991; Newman, 1991).

Effects of light and nutrient availability on the growth, allocation, carbon/nitrogen balance, phenolic chemistry, and resistance to herbivory of two freshwater macrophytes

Phenotypic responses of Potamogeton amplifolius and Nuphar advena to different light (7% and 35% of surface irradiance) and nutrient environments were assessed with field manipulation experiments. Higher light and nutrient availability enhanced the growth of P. amplifolius by 154% and 255%, respectively. Additionally, biomass was allocated differently depending on the resource: high light availability resulted in a higher root/shoot ratio, whereas high nutrient availability resulted in a lower root/shoot ratio. Low light availability and high nutrient availability increased the nitrogen content of leaf tissue by 53% and 40% respectively, resulting in a 37% and 31% decrease in the C/N ratio. Root nitrogen content was also increased by low light and high nutrient availability, by 50% (P=0.0807) and 77% respectively, resulting in a 20% and 40% decrease in root C/N ratio. Leaf phenolics were significantly increased 72% by high light and 31% by high nutrient availability, but root phenolic concentrations were not altered significantly. None of these changes in tissue constituents resulted in altered palatability to crayfish. N. advena was killed by the same high nutrient treatment that stimulated growth in P. amplifolius, preventing assessment of phenotypic responses to nutrient availability. However, high light availability increased overall growth by 24%, but this was mainly due to increased growth of the rhizome (increased 100%), resulting in a higher root/shoot ratio. High light tended to increase the production of floating leaves (P=0.09) and significantly decreased the production of submersed leaves. High light availability decreased the nitrogen content by 15% and 25% and increased the phenolic concentration by 88% and 255% in floating and submersed leaves, respectively. These differences in leaf traits did not result in detectable differences in damage by herbivores.

CRAYFISH FEEDING PREFERENCES FOR FRESHWATER MACROPHYTES: THE INFLUENCE OF PLANT STRUCTURE AND CHEMISTRY

Abstract The omnivorous crayfish Procambarus clarkii fed selectively on several species of macrophytes, preferring delicate fresh plants that had filamentous or finely-branched architectures. When the macrophytes were dried, powdered, and reconstituted into an alginate gel (thus eliminating among-species differences in physical characteristics), crayfish preferences were altered; previously tough plants that were high in nitrogen and protein were preferred over previously delicate plants that were low in nitrogen and protein. Even though plant structure influences feeding decision of crayfish, the structurally identical macrophyte gels were fed upon differently, demonstrating that nonstructural traits are important feeding determinants. However, plant tissue constituents such as nitrogen, protein, phenolics, lignin, cellulose, or ash were not significantly correlated with feeding preferences. Two high-nitrogen plants that were avoided by crayfish as fresh and as reconstituted tissue (Nuphar luteum macrophyllum and Alternanthera philoxeroides) possessed extracts that reduced crayfish feeding in laboratory assays, demonstrating that macrophyte metabolites can deter some herbivores. As is often observed with large generalist herbivores and omnivores in terrestrial and marine systems, the freshwater crayfish made feeding decisions based upon multiple plant cues (structure, nutrition, chemical defenses).

Chemical defenses, protein content, and susceptibility to herbivory of diploid vs. hapliod stages of the isomorphic brown alga Dictyota ciliolata (Phaeophyta).

Seaweeds with free-living diploid and haploid stages might express recessive traits during haploid stages, or exhibit other differences, that would allow those stages to differ in fitness under different environmental conditions. Heteromorphic seaweeds are well known to have variable ecological traits associated with their morphological differences, but ecological differences among isomorphic stages have rarely been investigated. The chemically defended brown alga Dictyota ciliolata has a life history with isomorphic alternation of generations, allowing us to assess how chemical traits and susceptibility to herbivory differ among stages. Herbivorous amphipods and sea urchins consumed similar amounts of diploid sporophytes and haploid female and male gametophytes. Concomitant with similar palatability, the different life stages had similar concentrations of soluble protein and levels of chemical defenses. Thus, in addition to morphological similarities, the life stages of D. ciliolata appear to share these ecological similarities.

A trophic cascade in a macrophyte-based food web at the land–water ecotone

Trophic cascades may purportedly be more common in aquatic than terrestrial food webs, but herbivory on freshwater vascular plants has historically been considered low. Water lilies are an exception, suffering severe grazing damage by leaf beetles. To test whether a central prediction of cascade models—that predator effects propagate downwards to plants—operates in a macrophyte-based food web, we experimentally manipulated predation pressure on a key herbivore of water lilies in the littoral zone of a lake in Michigan, USA. Field experiments comprised combinations of caging treatments to alter the number of predators (larvae of the ladybird beetle Coleomegilla maculata) that hunt the grazers of the macrophytes (larvae of the leaf beetles Galerucella nymphaeae) on the leaves of the water lily Nuphar advena. Predatory larvae of the ladybird beetles significantly reduced grazing damage to water-lily leaves by 35–43%. The predators reduced plant damage chiefly via density-mediated effects, when lower densities of grazers translated to significant declines in plant damage. Plant damage caused by the surviving herbivores was less than predicted from individual grazing rates under predator-free conditions. This suggests that trait-mediated effects may possibly also operate in this cascade. The observed strong effect of predators on a non-adjacent trophic level concurs with an essential component of the trophic cascade model, and the cascade occurred at the ecotone between aquatic and terrestrial habitats: Nuphar is an aquatic macrophyte with emergent and floating leaves, whereas both beetle species are semi-terrestrial and use the dry, emergent and floating leaves of the water lily as habitat. Also, the cascade is underpinned by freshwater macrophytes—a group for which trophic processes have often been underappreciated in the past.