Jeremy D. Long

Chemical cues induce consumer-specific defenses in a bloom-forming marine phytoplankton

Blooms of the phytoplankton Phaeocystis can comprise 85% of total production and generate major biogeochemical signals across broad oceanic regions. The success of Phaeocystis may result from its ability to change size by many orders of magnitude when it shifts from small cells of 4–6 μm to large colonies of up to 30,000 μm in diameter. Single cells are consumed by ciliates but not copepods, whereas colonies are consumed by copepods but not ciliates. We demonstrate that chemical cues associated with each of these grazers induce consumer-specific, but opposing, morphological transformations in the bloom-forming species Phaeocystis globosa. Chemical cues from grazing copepods suppress colony formation by a significant 60–90%, a response that should be adaptive because copepods feed four times more on colonies versus solitary cells. In contrast, chemical cues from grazing ciliates enhance colony formation by >25%, a response that should be adaptive because ciliates grow three times faster when fed solitary cells versus colonies. Because size-selective predation fundamentally alters community structure and ecosystem function, this chemically cued shift may redirect energy and nutrients from food webs supporting fisheries to those fueling detrital pathways, thus potentially altering ecosystem-level processes such as productivity, carbon storage, and nutrient release.

ASYMMETRIC COMPETITION VIA INDUCED RESISTANCE: SPECIALIST HERBIVORES INDIRECTLY SUPPRESS GENERALIST PREFERENCE AND POPULATIONS

Species may compete indirectly by altering the traits of a shared resource. For example, herbivore-induced responses in plants may make plants more resistant or susceptible to additional herbivorous insect species. Herbivore-induced plant responses can significantly affect interspecific competition and herbivore population dynamics. These herbivore-herbivore indirect interactions have been overlooked in aquatic ecosystems where previous studies used the same herbivore species to induce changes and to assess the effects of these changes. We asked whether seaweed grazing by one of two herbivorous, congeneric snail species (Littorina obtusata or Littorina littorea) with different feeding strategies and preferences would affect subsequent feeding preferences of three herbivore species (both snails and the isopod Idotea baltica) and population densities of three herbivore species (both snails and a third periwinkle snail, Lacuna vincta). In addition, we measured phlorotannin concentrations to test the hypothesis that these metabolites function as induced defenses in the Phaeophyceae. Snail herbivory induced cue-specific responses in apical tissues of the seaweed Fucus vesiculosus that affected the three herbivore species similarly. When compared to ungrazed controls, direct grazing by Littorina obtusata reduced seaweed palatability by at least 52% for both snail species and the isopod species. In contrast, direct grazing by L. littorea did not decrease seaweed palatability for any herbivore, indicating herbivore-specific responses. Previous grazing by L. obtusata reduced populations of L. littorea on outplanted seaweeds by 46% but had no effect on L. obtusata populations. Phlorotannins, a potential class of inducible chemicals in brown algae, were not more concentrated in grazed seaweed tissues, suggesting that some other trait was responsible for the induced resistance. Our results indicate that marine herbivores may compete via inducible responses in shared seaweeds. These plant-mediated interactions were asymmetric with a specialist (L. obtusata) competitively superior to a generalist (L. littorea).

Linking invasions and biogeography: Isolation differentially affects exotic and native plant diversity

The role of native species diversity in providing biotic resistance to invasion remains controversial, with evidence supporting both negative and positive relationships that are often scale dependent. Across larger spatial scales, positive relationships suggest that exotic and native species respond similarly to factors other than diversity. In the case of island habitats, such factors may include island size and isolation from the mainland. However, previous island studies exploring this issue examined only a few islands or islands separated by extreme distances. In this study, we surveyed exotic and native plant diversity on 25 islands separated by <15 km in Boston Harbor. Exotic and native species richness were positively correlated. Consistent with island biogeography theory, species richness of both groups was positively related to area and negatively related to isolation. However, the isolation effect was significantly stronger for native species. This differential effect of isolation on native species translated into exotic species representing a higher proportion of all plant species on more distant islands. The community similarity of inner harbor islands vs. outer harbor islands was greater for exotic species, indicating that isolation had a weaker influence on individual exotic species. These results contrast with recent work focusing on similarities between exotic and native species and highlight the importance of studies that use an island biogeographic approach to better understand those factors influencing the ecology of invasive species.

Local consumers induce resistance differentially between Spartina populations in the field

Intraspecific variation in the strength of inducible plant defenses plays a central role in the interactions between plants and herbivores. Studies of this variation are typically conducted in the greenhouse or laboratory rather than the field. We simultaneously manipulated densities of local consumers in the field within Maine and South Carolina populations of the smooth cordgrass Spartina alterniflora. South Carolina, but not Maine, plants induced resistance when grazed by local consumers. South Carolina populations of Littoraria snails and planthoppers colonized control more than previously grazed South Carolina plants, and Littoraria snails consumed more control than previously grazed plants. The inducible feeding deterrents in South Carolina plants appear to be water soluble, but not phenolic based. In contrast, grazed and control plants from Maine populations did not differ in attractiveness or palatability to Maine consumers. Thus, inducible plant responses by South Carolina plants had a strong effect on the South Carolina consumer community, but no analogous effect occurred in Maine. Field experiments are a powerful approach to detecting the strength of inducible plant resistance and its impacts on local consumers, which in this case were shown to vary with location.

Uniformity of Leaf Shelter Construction by Larvae of Epargyreus clarus (Hesperiidae), the Silver-Spotted Skipper

Larvae of the silver-spotted skipper, Epargyreus clarus (Hesperiidae), construct shelters from leaves of their leguminous host plants, making four distinct shelter types that change predictably over larval ontogeny. Shelters built by first-instar larvae are located on the apical half of the leaflet and are almost invariant in size, shape, and orientation, suggesting a stereotypical process of shelter location and construction. We have determined that the regularity of these shelters results from a prescribed pattern of larval movements and behaviors, in which larvae use their body length as a “ruler” and employ silk not only as a building material but also as a template to guide the location of cuts in the leaf. Though lepidopteran larvae lack the sensitive antennae, long jointed appendages, and other measurement devices used by structure-building bees, wasps, and caddis flies, they can nonetheless use simple tools and behavioral patterns to produce characteristic and regular shelters.

Community context mediates the top‐down vs. bottom‐up effects of grazers on rocky shores

Interactions between grazers and autotrophs are complex, including both top-down consumptive and bottom-up facilitative effects of grazers. Thus, in addition to consuming autotrophs, herbivores can also enhance autotroph biomass by recycling limiting nutrients, thereby increasing nutrient availability. Here, we evaluated these consumptive and facilitative interactions between snails (Littorina littorea) and seaweeds (Fucus vesiculosus and Ulva lactuca) on a rocky shore. We partitioned herbivores total effects on seaweeds into their consumptive and facilitative effects and evaluated how community context (the presence of another seaweed species) modified the effects of Littorina on a focal seaweed species. Ulva, the more palatable species, enhanced the facilitative effects of Littorina on Fucus. Ulva did not modify the consumptive effect of Littorina on Fucus. Taken together, the consumptive and facilitative effects of snails on Fucus in the presence of Ulva balanced each other, resulting in no net effect of Littorina on Fucus. In contrast, the only effect of Fucus on Ulva was to enhance consumptive effects of Littorina on Ulva. Our results highlight the necessity of considering both consumptive and facilitative effects of herbivores on multiple autotroph species in order to gain a mechanistic understanding of grazers top-down and bottom-up roles in structuring communities.

A tide prediction and tide height control system for laboratory mesocosms

Experimental mesocosm studies of rocky shore and estuarine intertidal systems may benefit from the application of natural tide cycles to better replicate variation in immersion time, water depth, and attendant fluctuations in abiotic and edaphic conditions. Here we describe a stand-alone microcontroller tide prediction open-source software program, coupled with a mechanical tidal elevation control system, which allows continuous adjustment of aquarium water depths in synchrony with local tide cycles. We used this system to monitor the growth of Spartina foliosa marsh cordgrass and scale insect herbivores at three simulated shore elevations in laboratory mesocosms. Plant growth decreased with increasing shore elevation, while scale insect population growth on the plants was not strongly affected by immersion time. This system shows promise for a range of laboratory mesocosm studies where natural tide cycling could impact organism performance or behavior, while the tide prediction system could additionally be utilized in field experiments where treatments need to be applied at certain stages of the tide cycle.

Herbivore impacts on marsh production depend upon a compensatory continuum mediated by salinity stress.

Plant communities are disturbed by several stressors and they are expected to be further impacted by increasing anthropogenic stress. The consequences of these stressors will depend, in part, upon the ability of plants to compensate for herbivory. Previous studies found that herbivore impacts on plants can vary from negative to positive because of environmental control of plant compensatory responses, a.k.a. the Compensatory Continuum Hypothesis. While these influential studies enhanced our appreciation of the dynamic nature of plant-herbivore interactions, they largely focused on the impact of resource limitation. This bias limits our ability to predict how other environmental factors will shape the impact of herbivory. We examined the role of salinity stress on herbivory of salt marsh cordgrass, Spartina foliosa, by an herbivore previously hypothesized to influence the success of restoration projects (the scale insect, Haliaspis spartinae). Using a combination of field and mesocosm manipulations of scales and salinity, we measured how these factors affected Spartina growth and timing of senescence. In mesocosm studies, Spartina overcompensated for herbivory by growing taller shoots at low salinities but the impact of scales on plants switched from positive to neutral with increasing salinity stress. In field studies of intermediate salinities, scales reduced Spartina growth and increased the rate of senescence. Experimental salinity additions at this field site returned the impact of scales to neutral. Because salinity decreased scale densities, the switch in impact of scales on Spartina with increasing salinity was not simply a linear function of scale abundance. Thus, the impact of scales on primary production depended strongly upon environmental context because intermediate salinity stress prevented plant compensatory responses to herbivory. Understanding this context-dependency will be required if we are going to successfully predict the success of restoration efforts and the ecological consequences of anthropogenic disturbances.

Density‐mediated indirect effects from active predators and narrow habitat domain prey

The hunting-mode-habitat-domain-range framework suggests that the mechanism driving trophic cascades (i.e., trait-mediated indirect interactions [TMIIs] vs. density-mediated indirect interactions [DMIIs]) should depend upon the functional traits of predators and prey. For example, trophic cascades containing active, broad habitat domain range (BHDR) predators interacting with narrow habitat domain range (NHDR) prey are predicted to arise primarily via TMIIs, because these prey should reduce their conspicuous activity in the presence of these predators. Unfortunately, this hypothesis is difficult to test given the strong bias against studies assessing trophic cascades containing NHDR prey. Furthermore, this hypothesis ignores evidence that (1) active predators can have high consumption rates on prey, (2) continuously responding to active predators foraging across broad areas is energetically costly for prey, and (3) cues from active, BHDR predators may not influence prey density. We examined the TMIIs and total indirect interaction (TII) produced during interactions between an active, BHDR ladybeetle predator (Naemia seriata) and its NHDR prey (scale insects). We exposed scale insects to nonlethal and lethal ladybeetle predators in laboratory mesocosms for 15 weeks. We measured the growth of the scale insects host plant (cordgrass) and the population density of scale insects. Contrary to theory, nonlethal ladybeetles did not induce TMIIs. However, lethal ladybeetles increased cordgrass total and root dry biomass by 36% and 44%, respectively, suggesting the presence of strong DMIIs. Additionally, both lethal and nonlethal ladybeetles reduced scale insect population density. Our findings suggest that DMIIs, rather than TMIIs, can result from interactions between active BHDR predators and NHDR prey.

Copper contamination impairs herbivore initiation of seaweed inducible defenses and decreases their effectiveness

Seaweed-herbivore interactions are often mediated by environmental conditions, yet the roles of emerging anthropogenic stressors on these interactions are poorly understood. For example, chemical contaminants have unknown consequences on seaweed inducible resistance and herbivore response to these defenses despite known deleterious effects of contaminants on animal inducible defenses. Here, we investigated the effect of copper contamination on the interactions between a snail herbivore and a brown seaweed that displays inducible resistance to grazing. We examined seaweed inducible resistance and its effectiveness for organisms exposed to copper at two time points, either during induction or after herbivores had already induced seaweed defenses. Under ambient conditions, non-grazed tissues were more palatable than grazed tissues. However, copper additions negated the preference for non-grazed tissues regardless of the timing of copper exposure, suggesting that copper decreased both how herbivores initiated these inducible defenses and their subsequent effectiveness. Copper decreased stimulation of defenses, at least in part, by suppressing snail grazing pressure—the cue that turns inducible defenses on. Copper decreased effectiveness of defenses by preventing snails from preferentially consuming non-grazed seaweed. Thus, contaminants can potentially stress communities by changing seaweed-herbivore interactions mediated via inducible defenses. Given the ubiquity of seaweed inducible resistance and their potential influence on herbivores, we hypothesize that copper contamination may change the impact of these resistant traits on herbivores.