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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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Susceptibility of invertebrate larvae to predators: how common are post-capture larval defenses?

(Georgia Institute of Technology, 1999-12-30) Bullard, Stephan G. ; Lindquist, Niels Lyle ; Hay, Mark E.

Predation is believed to be a major source of mortality for larvae of benthic invertebrates, but the palatability of larvae commonly found in the water column has rarely been assessed. Larval palatability assays were conducted by collecting live invertebrate larvae from a temperate field site and offering them to a suite of common predators (the fishes Lagodon rhomboides, Leiostomus xanthurus, and Monacanthus hispidus and the hard coral Oculina arbuscula). By crushing larvae that were rejected intact and re-offering them to predators, it was possible to distinguish between defenses based on morphological and chemical characteristics of the larvae. Additionally, abundance data were collected for taxonomic groups of larvae at our sampling location. The majority of invertebrate larvae were palatable to consumers. Most predators readily consumed polychaete larvae, barnacle nauplii, bivalve veligers, shrimp zoeae, crab megalopae, phoronid actinotrochs, and hemichordate tornaria (which together accounted for 65% of meroplankton abundance), suggesting that these larvae lacked effective morphological or chemical defenses. Against at least 1 fish predator, a significant number of gastropod veligers, barnacle cyprids, crab zoeae, and stomatopod larvae (which accounted for 34% of meroplankton abundance) appeared to be morphologically defended. Larvae from these groups tended to be rejected whole, but were consumed by fishes once they were crushed. A significant number of nemertean pilidia, asteroid bipinnaria, and cnidarian planulae (which accounted for only 0.2% of meroplankton abundance) were rejected both whole and crushed, suggesting that some species or individuals within these taxa may be chemically defended. Thus, the majority of larvae from this assemblage of temperate meroplankton lacked physical or chemical defenses against potential predators (3 fishes and 1 cnidarian). Among the remaining larvae, physical resistance to predators was much more common than chemical resistance.
Reduced mobility is associated with compensatory feeding and increased diet breadth of marine crabs

(Georgia Institute of Technology, 1999-11-03) Stachowicz, John J. ; Hay, Mark E.

Direct effects of predation have been widely recognized as important in affecting prey population dynamics and evolution. However, less attention has been devoted to the consequences of indirect effects of predators on prey behavior. For example, to avoid predation many animals restrict their activities to physical refugia and adopt low-mobility lifestyles, yet the consequences of these anti-predator behaviors for foraging and diet selection are relatively unknown. In this study we examine the relationships between mobility, feeding preferences, and compensatory feeding for 3 species of marine decapod crabs feeding on seaweeds in North Carolina, USA. Low mobility and high site fidelity of crabs were associated with a broad, non-selective diet and compensatory feeding. The majid Mithrax forceps exhibited the lowest mobility, highest site fidelity, and least selective diet of the 3 species, whereas another majid Libinia dubia was intermediate in both mobility and selectivity, and the xanthid Panopeus herbstii had the greatest mobility and narrowest diet. Of these 3 crabs, only M. forceps compensated for low food quality by increasing consumption rates in single food-species feeding assays. This may be because M. forceps is resistant to (or tolerant of) seaweed chemical defenses, while other crab species are not. The ability to consume, and presumably subsist on, a wide variety of potential foods including those defended from more mobile consumers may facilitate a low-mobility lifestyle, allowing the crab to minimize movement and reduce exposure to predators. Low mobility and high site-fidelity may thus facilitate the formation and use of associational refuges with sessile benthic organisms that are resistant to predators; these associations can have important community and ecosystem-wide consequences.
Mutualism and coral persistence: the role of herbivore resistance to algal chemical defense

(Georgia Institute of Technology, 1999-09) Stachowicz, John J. ; Hay, Mark E.

Because seaweeds uncontrolled by herbivores can overgrow and kill corals, competition can exclude corals from temperate latitudes where herbivores generally fail to control seaweed biomass. In this study, we show that the coral Oculina arbuscula persists on reefs in temperate North Carolina where seaweeds are common by harboring the omnivorous crab Mithrax forceps, which removes seaweeds and invertebrates growing on or near the coral. In the field, corals from which crabs are experimentally removed develop a dense cover of epibionts, exhibiting reduced growth and increased mortality relative to corals with crabs, which remain epibiont-free. This crab is unusual in that it readily consumes all local seaweeds in laboratory choice assays and is not deterred by chemical defenses that suppress feeding by local fishes, sea urchins, and other crabs. This allows Mithrax to defend corals from overgrowth by chemically noxious seaweeds like Dictyota and Sargassum that are avoided by most local herbivores. However, further field manipulations under reduced light conditions demonstrate that the outcome of the crab–coral interaction is context-dependent: crabs only benefit corals in well-lit areas where seaweeds are abundant. Field observations and tethering experiments show that, by living in association with Oculina, Mithrax gains a refuge from predation. Additionally, crabs grow faster when associated with live corals than with structurally equivalent dead corals, apparently because they are able to consume lipid-rich coral mucus. This mucus provides a dietary supplement that may help corals attract and retain low-mobility symbionts such as Mithrax, securing for the coral long-term and predictable protection against competitors. Structurally complex but competitively inferior organisms, like some corals and coralline algae, provide the biogenic habitat complexity upon which many other species depend. Because these sessile organisms may be dependent on symbionts to remove superior competitors, mutualisms can play an important, but currently underappreciated, role in structuring marine communities where biotic interactions are intense. In this study, the mutualism between Oculina and Mithrax promotes the persistence of both species in habitats from which they might otherwise be excluded by competition and predation.
Reducing predation through chemically mediated camouflage: indirect effects of plant defenses on herbivores

(Georgia Institute of Technology, 1999-03) Stachowicz, John J. ; Hay, Mark E.

Herbivores often specialize on particular hosts that provide both food and shelter from natural enemies. It is thus often unclear whether a plant’s value as a food or its value as a safe shelter has played a larger role in selecting for specialization. Decorator crabs offer a novel opportunity to investigate the relative effects of diet vs. natural enemies in selecting for specialization because these crabs place plant “shelter” on their backs as camouflage but need not use these plants as food, thus decoupling the plant’s value as a food from its value as a shelter. In this study, we show that juveniles of the decorator crab Libinia dubia selectively decorate with the chemically defended brown alga Dictyota menstrualis but treat this plant as a low-preference food. Common omnivorous fishes that are potential predators of Libinia avoid consuming Dictyota due to the alga’s potent chemical defenses. In the field, juvenile crabs decorated with Dictyota experience significantly less predation than crabs decorated with an alga that is not chemically noxious to local fishes, and the Dictyota metabolite that most strongly deters feeding by fishes is the specific metabolite that determines decoration choice by this crab. Thus, by behaviorally sequestering defenses from this chemically noxious plant, these small crabs reduce their susceptibility to predation. In the presence of predators, juvenile crabs reduce their rate of feeding, but not of decorating, suggesting that antipredator behavior such as decorating takes precedence over feeding. In addition, only juvenile crabs that are of a size that can be consumed by local fishes decorate at all. Adult crabs that have carapace widths exceeding the gape size of co-occurring fishes do not decorate in either the field or the laboratory. Apparently predation, rather than diet selection, drives decoration specialization in Libinia, highlighting how indirect effects of plant secondary chemistry can impact herbivore behavior, ecology, and evolution.
Induction of seaweed chemical defenses by amphipod grazing

(Georgia Institute of Technology, 1996-12) Cronin, Greg ; Hay, Mark E.

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 significantly 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. longimana 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 defenses, 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. longimana 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.
Are tropical plants better defended? Palatability and defenses of temperate vs. tropical seaweeds

(Georgia Institute of Technology, 1996-12) Bolser, Robin C. ; Hay, Mark E.

Investigators working in both terrestrial and marine systems hypothesize that prey defenses are better developed in tropical than in temperate habitats because tropical consumers are more active and diverse. To investigate the hypothesis that chemical defenses are more potent in tropical than in temperate seaweeds, we conducted 38 feeding assays involving seven genera of algae. We offered tropical and temperate sea urchins the choice of a temperate alga from North Carolina or a closely related tropical alga from the Bahamas. Plants were freeze—dried, ground to a fine powder, embedded in agar, and presented in congeneric pairs (North Carolina species vs. Bahamian species), or same—species pairs, to the temperate urchin Arbacia punctulata and the tropical urchin Lytechinus variegatus. For the genera we tested (the red alga Amphiroa, the green alga Udotea, and the brown algae Dictyopteris, Dictyota, Lobophora, Padina, and Sargassum), we documented a general pattern in which the mean amount of North Carolina seaweeds eaten was approximately twice that of their Bahamian congeners. Dictyota was an exception to the overall pattern, in that mean consumption of temperate and tropical species was equivalent. In addition to showing a latitudinal difference in seaweed palatability, we found that some species exhibited significant, between—population variation in herbivore resistance on a local scale. The most notable example was Dictyota menstrualis from North Carolina. When collected from a shallow inshore site, this species was significantly more palatable than tropical species of Dictyota in four of six contrasts. When collected from a deeper offshore site, it was significantly less palatable than the tropical species in four of six contrasts. Thus, for this species, the between—population variance in palatability within a geographic region (North Carolina) bracketed the variance in palatability that we found among species and between regions. Feeding assays with both temperate and tropical urchins produced similar results, indicating that choices were made based on fundamental characteristics of the algae rather than on greater familiarity with local prey species. To see if chemical defenses could explain the differences in herbivore resistance that we noted using freeze—dried algae, we tested the effects of lipid—soluble and water—soluble extracts from each alga on urchin feeding by incorporating extracts into a standard palatable food. We also measured protein content and percent ash—free dry mass of the seaweeds in order to correlate urchin feeding preferences with these measures of food quality. Lipophilic chemical extracts explained urchin preferences in 9 of 15 (60%) North Carolina—Bahamas contrasts. Water—soluble extracts, protein content, and percent ash—free dry mass generally did not account for feeding patterns seen in the original assays. Our results support the general hypothesis that tropical seaweeds have stronger chemical defenses than temperate seaweeds. For some genera, however, smaller—scale local variability in herbivore resistance within a species can be as striking as overall latitudinal differences.
Palatability and chemical defenses of marine invertebrate larvae

(Georgia Institute of Technology, 1996-11) Lindquist, Niels Lyle ; Hay, Mark E.

Risk of larval mortality is a critical component of models and debates concerning the ecology and evolution of the differing reproductive characteristics exhibited by marine invertebrates. In these discussions, predation often is assumed to be a major source of larval mortality. Despite limited empirical support, most marine larvae are thought to be palatable and broadly susceptible to generalist predators. Previous studies of larval—planktivore interactions have focused primarily on larvae that typically feed, grow, and develop for weeks to months in the plankton. Such planktotrophic species commonly produce large numbers of small larvae that disperse over vast distances. In contrast, the nonfeeding lecithotrophic larvae from sessile invertebrates that brood are often large and conspicuous, lack morphological defenses, and have limited dispersal distances because they typically are competent to settle minutes to hours after spawning. Interactions between lecithotrophic larvae and consumers are not well studied. This has limited the ability of previous authors to test broad generalities about marine larvae. We show that brooded larvae of Caribbean sponges (11 species) and gorgonians (three species) as well as brooded larvae of temperate hydroids (two species) and a bryozoan are unpalatable to co—occurring fishes. In contrast, brooded larvae of temperate ascidians (three species), a temperate sponge, and Caribbean hard corals (three species) are readily consumed by fishes, as are larvae from four of six species of synchronous broadcast—spawning gorgonians from the Florida Keys. Frequencies of survivorship for larvae attacked and rejected by fishes were high and statistically indistinguishable from frequencies for unattacked control larvae. Frequency of metamorphosis (when it occurred) of rejected larvae never differed significantly from that of unattacked control larvae. Assays testing for larval vs. adult chemical defenses for five species with distasteful larvae showed that larvae of all five species were chemically distasteful to fishes, whereas only three of five adult extracts deterred fish feeding. A comparison of larval palatability among chemically rich taxa showed that brooded larvae were significantly more likely to be unpalatable (86% of the species tested) than larvae of broadcasters (33%), and that palatable larvae were rarely released during the day (23%) while unpalatable larvae usually were (89%). Additionally, the frequency of bright coloration was high (60%) for unpalatable larvae and low (0%) for palatable larvae, suggesting that unpalatable larvae often may be aposematically colored. Results of this broad survey cast doubt on the widely accepted notion that virtually all marine larvae are suitable prey for most generalized planktivores. Among species that do not chemically or physically protect larvae against fishes, selection appears to favor the release of larvae at night, or the production of smaller more numerous offspring that grow and develop at sea as a way of escaping consumer—rich benthic habitats. Because distasteful larvae are not similarly constrained, distasteful species should exhibit reproductive and larval characteristics selected more by the fitness—related consequences of larval development mode and dispersal distance than by the necessity of avoiding benthic predators. Production of large larvae and retention of offspring in parental habitats that have proved to be suitable for growth and reproduction have both been proposed as advantageous, but these advantages often were assumed to be offset by losses due to increased larval apparency to fishes. This assumed trade—off is not mandatory because larvae can be defended chemically. Distasteful larvae tend to be conspicuous, localized dispersers that can co—occur with benthic fishes, and yet not be consumed.
Defensive synergisms?: Reply to Pennings

(Georgia Institute of Technology, 1996-09) Hay, Mark E.
Coral-seaweed-grazer-nutrient interactions on temperate reefs

(Georgia Institute of Technology, 1996-08) Miller, Margaret W. ; Hay, Mark E.

Why corals dominate tropical reefs but are rare or absent on temperate reefs is one of the more intriguing global—scale questions in marine ecology. Restriction of corals from temperate reefs has been suggested to be due to low temperature, competition with seaweeds, and synergistic interactions of physical and biological factors. However, most studies addressing these hypotheses have been non—experimental and conducted on tropical corals and reefs near the extremes of their distribution rather than in temperate habitats using corals that are physiologically suited to temperate environments. Some corals occur only in temperate regions, but their ecology is largely unstudied. In an attempt to understand how temperate corals function at latitudes where corals are relatively rare and where reefs tend to be dominated by seaweeds, we examined responses of the temperate coral Oculina arbuscula to competition with seaweeds on reefs in North Carolina (USA). We asked how competitive interactions were affected by levels of grazing, nutrients, or interactions of these factors. Sampling of 12 reef habitats ranging from 1 m deep, inshore sites to 25 m deep, offshore sites demonstrated a strong negative relationship between percentage cover of seaweeds and density of Oculina colonies. Seaweeds dominated well—lit habitats (shallow inshore reefs or deep offshore reefs with clear waters), while coral was significantly more abundant in low—light habitats where seaweeds were rare (deep inshore habitats or nearshore reefs with turbid waters). This general among—site pattern also occurred within an individual site as one moved from shallow, well—lit waters to deeper, darker waters. Corals transplanted into seaweed—dominated areas grew well if seaweed canopies were removed but grew poorly, or not at all, if canopies were left intact. Seaweeds also significantly inhibited recruitment of O. arbuscula. At a turbid inshore reef, recruitment was high at a depth of 6 m where seaweeds were rare, but very low at a depth of 1 m where seaweeds were abundant. Removal of seaweeds from shallow plots increased recruitment about 12—fold to levels that did not differ significantly from those at 6 m. In grazer—exclusion cages on offshore reefs, Oculina recruitment varied significantly between sites and years. Almost no recruitment was observed at a well—lit, plant—dominated site while recruitment was higher, to very high, at a turbid site with few seaweeds. At this turbid site, recruitment was facilitated by grazing but could not be related to grazer effects on seaweeds. Facilitation was apparently due to consumers removing barnacles, which dominated this low—light site if grazers were excluded. Cage exclusion of larger herbivores at two offshore sites (primarily fishes) and one inshore site (fishes and urchins) had no significant effect on coral growth. At the well—lit inshore site, herbivores had a large effect on the species composition of the seaweed community, but little effect on the total abundance of seaweeds. Large grazers caused palatable red seaweeds to be replaced by similar amounts of unpalatable brown seaweeds. Therefore, herbivory alone had little impact on total seaweed abundance and the levels of seaweed competition affecting co—occurring O. arbuscula. In contrast, when we conducted a factorial experiment manipulating both herbivory and nutrient levels, exclusion cages significantly reduced coral growth. In this experiment, nutrient addition had no effect on brown seaweeds but significantly increased the percentage cover of red seaweeds in exclusion cages. Nutrient addition also tended to suppress coral growth in herbivore—exclusion cages where red seaweeds were stimulated, but to increase coral growth in open cages where herbivores had removed the red seaweeds. Thus, nutrients and herbivory may have acted synergistically to affect seaweeds, and hence corals, on this temperate reef. Different groups of algae (red vs. brown) experienced differential degrees of nutrient limitation and exerted differential competitive effects on corals at this site. Our findings show that competition with seaweeds plays a large role in excluding Oculina from well—lit temperate reefs, and support the hypothesis that seaweed competition may interact with latitudinal changes in physical parameters to limit coral recruitment, growth, and accumulation at high latitudes, thus suppressing the potential for reef development.
Susceptibility to herbivores depends on recent history of both the plant and animal

(Georgia Institute of Technology, 1996-07) Cronin, Greg ; Hay, Mark E.

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 metabolites 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.