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Hay, Mark E.

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https://hdl.handle.net/1853/71334

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School of Biological Sciences

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Strong impacts of grazing amphipods on the organization of a benthic community

(Georgia Institute of Technology, 2000-05) Duffy, J. Emmett ; Hay, Mark E.

Large brown seaweeds dominate coastal hard substrata throughout many of the world's 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 seaweeds, 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 amphipods were attributable largely, if not exclusively, to the single amphipod species Ampithoe 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 grazer's 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 amphipods, 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 resistance to seaweed chemical defense: the roles of herbivore mobility and predation risk

(Georgia Institute of Technology, 1994-07) Duffy, J. Emmett ; Hay, Mark E.

Numerous small sedentary herbivores (mesograzers such as amphipods, small crabs, and gastropods) are resistant to seaweed secondary metabolites that deter larger, more mobile herbivorous fishes. In addition, specialist mesograzers experience reduced predation from fishes when living on seaweeds that produce these compounds. In this study we tested the hypothesis that generalist, as opposed to specialist, mesograzers can also benefit from reduced predation when they occupy chemically defended plants. Secondly, we assessed the hypothesis that low herbivore mobility, unconfounded by herbivore size or specialized feeding, selects for tolerance of seaweed chemical defenses, by comparing responses to the chemically defended brown seaweed Dictyota menstrualis of three sympatric, generalist amphipods that differ in mobility (Ampithoe longimana, Ampithoe valida, and Gammarus mucronatus). Response to Dictyota's chemical defenses varied as much among these three amphipods as among the phylogenetically distant fishes and mesograzers studied previously and supported the hypothesis that less mobile herbivores should be most tolerant of plant chemical defenses. In laboratory experiments, A. longimana moved little, preferentially consumed Dictyota over other seaweeds, and was unaffected by all Dictyota secondary metabolites tested. In contrast, G. mucronatus was active, it did not feed on Dictyota, and two of three Dictyota secondary metabolites deterred its grazing. Distribution of amphipods in the field suggested that these feeding patterns affected amphipod risk of predation. A. longimana reached its highest abundance on Dictyota, which is unpalatable to omnivorous fish predators, during the season when fish are most abundant. At the same time, the highly active G. mucronatus decreased to near extinction. Like G. mucronatus, A. valida was detterred by two Dictyota secondary metabolites, did not eat Dictyota, and disappeared when fishes were abundant. Experiments confirmed that A. longimana was less vulnerable to fish predation when occupying a chemically defended seaweed than when occupying a palatable seaweed. This decreased predation resulted primarily from a decreased frequency of encounter with predators when amphipods were on chemically defended plants. When we experimentally equalized encounter rates between omnivorous pinfish (Lagodon rhomboides) and the seaweed Dictyota menstrualis and Ulva curvata (unpalatable and palatable, respectively, to pinfish) in the laboratory, amphipods occupying these two plants were eaten at similar rates. In contrast, when live amphipods were affixed to Ulva and Dictyota and deployed in the field, amphipods survived only on Dictyota. Heavy fish grazing on Ulva in the latter experiment suggests that poor survival of amphipods on Ulva may have resulted from greater detection and/or incidental ingestion of amphipods on this plant, due to frequent visitation by fishes. Infrequent visitation of Dictyota by foraging fish also may explain A. longimana's persistence through the summer on this chemically defended seaweed while the two Ulva—associated amphipods declined precipitously. These results (1) confirm that association with chemically defended plants can reduce predation on generalist, as well as specialist, herbivores and (2) suggest that preferential feeding on chemically defended plants is most likely for sedentary mesograzers because low mobility enhances the ability to exploit chemically defended seaweeds as refuges from fish predation.
Food and shelter as determinants of food choice by an herbivorous marine amphipod

(Georgia Institute of Technology, 1991) Duffy, J. Emmett ; Hay, Mark E.

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 ofthe herbivorous marine amphipodAmpithoe iongimana. When offered a choice offive common seaweeds, this amphipod fed most readily on Dietyota and Hypnea and less readily on Sargassum, Chondria, and Caionitophyllum. 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. iongimana 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. iongimana was more abundant on Dietyota and Sargassum (both unpalatable to omnivorous fishes), than on Hypnea, Chondria, and Caionitophyllum (all of which are palatable to fishes). During the season when omnivorous fishes were abundant, density of A. iongimana increased on Dietyota, 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. iongimana among seaweeds, since there were no negative correlations between A. iongimana abundance and total amphipod abundance 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 reproduction, suggests that host-plant use by A. iongimana may be strongly constrained by requirements for shelter from predation.
Amphipods are not all created equal: a reply to Bell

(Georgia Institute of Technology, 1991) Duffy, J. Emmett ; Hay, Mark E.

In laboratory feeding trials, Hay et al. (1987) found that the tube-building amphipod Ampithoe longimana readily consumed the brown seaweed Dictyota dichotorna, which was not eaten by local fish. The diterpene alcohols pachydictyol A and dictyol E, which are produced by this species of Dictyota, significantly deterred feeding by fish but either stimulated or did not affect feeding by the amphipod. Based on these data, Hay et al. (1987) suggested that small, relatively sedentary mesograzers like the amphipod they studied might experience decreased predation if they lived on seaweeds that were chemically defended and thus not commonly consumed or visited by omnivorous or herbivorous fishes. Because predation is a major source of mortality for amphipods and other mesograzers (see references in Hay et al. 1987), they reasoned that selection might favor sedentary mesograzers that could live on and eat chemically defended seaweeds.
Seaweed Adaptations to Herbivory

(Georgia Institute of Technology, 1990-05) Duffy, J. Emmett ; Hay, Mark E.
Host-plant specialization decreases predation on a marine amphipod: an herbivore in plant's clothing

(Georgia Institute of Technology, 1990) Hay, Mark E. ; Duffy, J. Emmett ; Fenical, William

We investigated the factors selecting for host-plant specialization and the roles that plant defensive chemistry may play in this process. We studied marine organisms because marine communities contain fewer specialized herbivores than terrestrial communities and, therefore, provide a simplified system for investigating certain aspects of host-plant specialization. Our study focused on the unusual domicile-building and feeding behavior of the amphipod Pseudamphithoides incurvaria, which is the only herbivorous marine amphipod known to specialize on a few closely related seaweeds. P. incurvaria lives in a portable, bivalved domicile that it constructs from the chemically defended brown alga Dictyota bartayresii. Chemical assays indicate that natural populations of Pseudamphithoides construct their domiciles from D. bartayresii even when this alga is rare compared to other Dictyota species and to other related genera in the family Dictyotaceae. In both choice and no-choice tests in the laboratory, Pseudamphithoides built domiciles from and selectively consumed species of Dictyota that produced dictyol-class diterpenes that deter feeding by reef fishes. Other brown seaweeds in the family Dictyotaceae, including a Dictyota species, that did not produce these fish-feeding deterrents were avoided by the amphipod. Amphipods removed from their domiciles were rapidly eaten when presented to predatory fish; amphipods in their normal domiciles were consistently rejected by fish. The defensive value of the domicile appeared to result from specific characteristics of the Dictyota from which it was built, since amphipods forced to build domiciles from the palatable green seaweed Viva were rapidly eaten when these amphipods, in their domiciles, were exposed to predatory fish. Algal defensive chemistry directly cued domicile building. When the green alga VIva was treated with pachydictyol-A (the major secondary metabolite produced by Dictyota bartayresiz), domicile building by Pseudamphithoides increased in proportion to the concentration of pachydictyol-A. All data collected during this study are consistent with the hypothesis that predator escape and deterrence are primary factors selecting for host specialization by Pseudamphithoides incurvaria. Similar conclusions can be drawn for the limited number of other marine herbivores that are relatively specialized.
Chemical defense in the seaweed Dictyopteris delicatula: differential effects against reef fishes and amphipods

(Georgia Institute of Technology, 1988-09-21) Hay, Mark E. ; Duffy, J. Emmett ; Fenical, William ; Gustafson, Kirk

Many seaweeds produce chemicals that deter feedlng by fishes and sea urchins. A growing body of evidence suggests that small, relatively immobile herbivores (mesograzers) such as amphpods, polychaetes, and ascoglossan gastropods are often unaffected by these compounds and may preferentially consume seaweeds that are chemically defended from fishes. We tested this hypothesis by examining the responses of reef fishes and amphipods to a mutture of 2 C,, hydrocarbons, &ctyopterenes A and B, produced by the Canbbean brown alga D~ctyopteris delicatula. This alga was intermediate in preference for reef fishes, and the dictyopterenes reduced fish grazing by a significant 40 %. In contrast, D. delicatula was highly preferred by a muted-species group of amphipods and the dlctyopterenes had no effect on their feeding Despite the tendency for mesograzers to selectively consume some seaweeds that are chemically deterrent to fishes, true specialization by these or other marine herbivores appears to be rare in companson with terrestnal systems. Plant-dwelling amphipods at our study site in the Grenadine Islands were found on, and consumed a variety of, macrophytes; they were not restrict~velys pecialized to D. delicatula. Many terrestnal insects are very specialized feeders, sequester toxins from theu food plants, and use these as duect defenses against predation. In contrast, sequestenng of seaweed toxlns by marine mesograzers appears to be relahvely rare. However, the indirect advantage of llving on seaweeds that are not eaten by fishes may be considerable. We hypothesize that mesograzers living on plants chemically defended from fishes wlll experience less predation than those living on plants preferred by fishes.
Chemical defense against different marine herbivores: are amphipods insect equivalents?

(Georgia Institute of Technology, 1987) Hay, Mark E. ; Duffy, J. Emmett ; Pfister, Catherine A. ; Fenical, William

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 ofthe palatable seaweed Graci/aria 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 playa major role in determining its susceptibility to herbivores. The ability of amphipods to circumvent the chemical defenses of 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 may be under very different evolutionary constraints than the larger, more mobile herbivores that commonly move 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.