Diterpene alcohols produced by the brown seaweed Dictyota menstrualis deter feeding by numerous species of abundant herbivores. Here we show that these same compound also may prevent fouling organisms from colonizing the surface of this alga. In the field, Dictyota menstrualis plants were less frequently and less heavily fouled than any of the other common seaweed species investigated. In laboratory assays, larvae of the common fouling bryozoan Bugula neritina failed to settle on Dictyota even though they contacted its surface as often as they contacted the surface of a preferred host alga. Rejection occurred only after direct contact with the alga's surface. Rejection of Dictyota was not mediated by water—borne chemical cues or by surface wettability (a physical property of the surface that can affect fouling). The lipid—soluble extract from surface rubbings of Dictyota inhibited larval settlement when placed on other surfaces and contained the diterpene alcohols pachydictyol A and dictyol E. Larvae exposed to these compounds experienced mortality, abnormal development, or reduced rates of development. Although the potential for chemically mediated coevolution between plants and herbivores has been the focus of scores of previous investigations, such coevolution will depend on selection altering the chemical defenses of the plant following the evolution of resistance by herbivores. Such a reciprocal response will be constrained if compounds play multiple roles that are ecologically important. Dictyota produces secondary metabolites that are broadly defensive against a wide variety of consumers and fouling organisms. Although certain consumers may evolve resistance to these metabolites, it is unclear that feeding by these consumers will result in reciprocal responses from the plant. We suggest that coevolved interactions may be uncommon, and that many interactions that appear to be coevolved may result from fortuitous and opportunistic preadaptations.
Genetic variation in tolerance for seaweed chemical defenses among populations of marine herbivores is poorly described, either because few marine studies have addressed the issue or because the feeding preferences of populations of marine herbivores rarely differentiate. We address this using the polyphagous amphipod Ampithoe longimana (Crustacea), which commonly consumes, and lives on, terpene-rich brown seaweeds in the tropical genus Dictyota. Previous work demonstrated that in areas where the amphipod and seaweeds overlap geographically, these chemically deterrent seaweeds provide the amphipod with spatial refuges from predation by omnivorous fishes that avoid consuming Dictyota. However, the amphipod's distribution extends northward of the seaweed's distribution, making this benefit of association unavailable to more northerly populations of amphipods. On average, populations sympatric with Dictyota have stronger feeding preference for Dictyota species and greater fitness when raised on Dictyota than do populations that are outside Dictyota's geographic endpoint. These results are consistent with the hypothesis that in areas where the amphipods co-exist with Dictyota, selection favors amphipods that tolerate Dictyota's chemical defenses and thereby access its enemy-free space. Amphipods allopatric with Dictyota are unable to tolerate Dictyota's chemical defenses, either because of selection, drift, or some mix of both forces. A trade-off between preference for Dictyota and for the chemically distinct seaweed Hypnea musciformis is suggested by the finding that populations with high preference for Dictyota tended to have lower preference for Hypnea. However, this population-level pattern appears to be the result of independent evolution and not a genetic trade-off: an analysis of full-sib families within a single population detected heritable variation in preferences for Dictyota and suggested this for Hypnea (although the latter was not statistically significant), yet no family-level covariation was detected. Phylogeographic analysis of mitocondrial DNA and nuclear sequences indicates a strong historical break between populations sympatric with Dictyota and populations more than 500 km beyond Dictyota's geographic endpoint. The historical separation of these most northerly populations could have allowed a random accumulation of alleles to effectively degrade tolerance for Dictyota, although selection may also be responsible for the degradation.
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 of 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 abundant 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 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. longimana may be strongly constrained by requirements for shelter from predation.
A table showing the collection sites for both the live and freeze-dried data sets.
Chapter 3. The Role of Seaweed Chemical Defenses in the Evolution of Feeding Specialization and in the Mediation of Complex Interactions was published in Ecological Roles of Marine Natural Products on page 93.
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.
MEPS Marine Ecology Progress Series Contact the journal Facebook Twitter RSS Mailing List Subscribe to our mailing list via Mailchimp HomeLatest VolumeAbout the JournalEditorsTheme Sections MEPS 218:249-266 (2001) - doi:10.3354/meps218249 Macroalgal traits and the feeding and fitness of an herbivorous amphipod: the roles of selectivity, mixing, and compensation Edwin Cruz-Rivera1, Mark E. Hay2,* 1University of Guam Marine Laboratory, UOG Station, Mangilao, Guam 96923, USA 2School of Biology, Georgia Institute of Technology, Atlanta, Georgia 30332-0230, USA *Corresponding author. E-mail: mark.hay@biology.gatech.edu ABSTRACT: Selective feeding, compensatory feeding, and diet mixing have all been proposed as adaptive strategies allowing herbivores to enhance nutrient intake from low quality plant and algal foods. However, little is known about the relative importance of these alternative feeding strategies for consumer fitness or about how these strategies are affected by prey nutritional traits. To address this, we studied the effects of algal nutritional value and toughness on feeding choices, feeding rates, and survival, growth and fecundity of the amphipod Ampithoe longimana. To assess the value of diet mixing, we compared fitness of amphipods cultured on each of 15 algal species or on 4 different mixtures of algae. We also quantified how sequentially switching between algae that supported higher and lower fitness affected fitness compared to monospecific diets of these algae and to a constant mixture of the algae. Protein, nitrogen, organic content, or toughness of algae did not correlate with food choice by A. longimana. In contrast, we found a strong inverse correlation between feeding rates and algal organic content [ash free dry mass/wet mass (AFDM:WM) and total organic carbon (TOC)], and, to a lesser extent, protein (but not nitrogen). Thus, when confined with algae having lower nutritional value, A. longimana used quantity to compensate for quality. This compensatory feeding was confirmed by feeding amphipods on artificial diets that varied only in their amount of AFDM:WM. Despite broad differences in algal nutrient content or other traits, compensatory feeding allowed this amphipod to maintain high fitness when cultured on most, but not all, algae. Access to algal mixtures did not enhance fitness compared to feeding on several algae offered alone, suggesting that A. longimana need not rely on a mixed diet. Even when significant differences in survivorship or growth occurred between a monospecific diet and a mixed diet, fecundity or size of eggs produced by egg-bearing survivors were generally unaffected. Furthermore, when amphipods were switched sequentially (every 24 h) between 2 different quality algae, only growth (but not survivorship, fecundity, or egg size) was affected, with growth determined primarily by the higher quality alga offered. Amphipods confined with the green alga Codium fragile ovulated significantly later than conspecifics on one mixed diet, but this effect was observed only in 1 of 2 long-term assays. Thus, dietary mixing offered only a moderate benefit to this amphipod under very restrictive conditions. For A. longimana, food selection is relatively unresponsive to algal nutritional quality, apparently because compensatory feeding allows this amphipod to successfully exploit a variety of algal foods. Compensatory feeding also may reduce the need to move among host algae in order to mix diets, thus decreasing the risk of movement-associated detection by predators. KEY WORDS: Ampithoe longimana · Compensatory feeding · Diet mixing · Dietary effects on fitness · Herbivore food choice · Mesograzers · Alga nutritional quality Full text in pdf format PreviousNextExport citation RSS - Facebook - Tweet - linkedIn Cited by Published in MEPS Vol. 218. Online publication date: August 20, 2001 Print ISSN: 0171-8630; Online ISSN: 1616-1599 Copyright © 2001 Inter-Research.
