Conspecific cues, not starvation, mediate barren urchin response to predation risk.

Prey state and prey density mediate antipredator responses that can shift community structure and alter ecosystem processes. For example, well-nourished prey at low densities (i.e., prey with higher per capita predation risk) should respond strongly to predators. Although prey state and density often co-vary across habitats, it is unclear if prey responses to predator cues are habitat-specific. We used mesocosms to compare the habitat-specific responses of purple sea urchins (Strongylocentrotus purpuratus) to waterborne cues from predatory lobsters (Panulirus interruptus). We predicted that urchins from kelp forests (i.e., in well-nourished condition) tested at low densities typically observed in this habitat would respond more strongly to predation risk than barren urchins (i.e., in less nourished condition) tested at high densities typically observed in this habitat. Indeed, when tested at densities associated with respective habitats, urchins from forests, but not barrens, reduced kelp grazing by 69% when exposed to lobster risk cues. Barren urchins that were unresponsive to predator cues at natural, high densities suddenly responded strongly to lobster cues when conspecific densities were reduced. Strong responses of low densities of barren urchins persisted across feeding history (i.e. 0-64 days of starvation). This suggests that barren urchins can respond to predators but typically do not because of high conspecific densities. Because high densities of urchins in barrens should weaken the non-consumptive effects of lobsters, urchins in these habitats may continue to graze in the presence of predators thereby providing a feedback that maintains urchin barrens.

Geographic variation in the sensitivity of an herbivore-induced seaweed defense.

Intraspecific variation in primary producer induced defenses may affect how these defenses contribute to population and community regulation. For instance, inducible defenses may play larger roles in primary producer populations that are sensitive to low levels of grazing than populations that only respond to high levels of grazing. Although the incidence of herbivore-induced defenses is well documented, and there are examples of geographic variation in these defenses, we have limited knowledge of the factors that affect sensitivity to grazing (i.e., the minimum grazer density needed to elicit these responses) within and among populations. Filling this gap is necessary to understand the importance of these defenses under different conditions. To address whether the sensitivity of seaweed induced defenses varies geographically, we exposed Northern and Southern California populations of the seaweed Silvetia compressa to five densities of the snail Tegula funebralis, under ambient, regional environmental conditions. Southern seaweeds required high levels of grazing to induce defenses, while all levels of herbivory decreased Northern seaweed palatability. To better understand these different responses to low levels of grazing, we conducted common garden experiments to directly test the roles of experimental environment and herbivore source. Consistent with initial experiments, Northern Silvetia responded to low levels of grazing, regardless of environmental conditions, while Southern Silvetia never responded to low levels of grazing, even after being acclimated to Northern environmental conditions for 24 d. Additionally, Southern Silvetia did not respond to grazing by Northern snails, suggesting that herbivore source did not explain this geographic pattern in inducible seaweed defenses. Together, these observations suggest that the seaweed source explains this geographic pattern in sensitivity. Trade-offs with constitutive defenses did not help explain this pattern, as Southern Silvetia had weaker constitutive defenses than Northern seaweeds. This may be due to a combination of low grazing pressure and low predictability of attack in the South. Thus, population variation in sensitivity may be due to long-term differences in environmental histories, resulting in local adaptation or legacy effects from exposure to local conditions. Overall, our results indicate that these herbivore-induced responses may be more important in Northern Silvetia populations than Southern ones.

Fish predators reduce kelp frond loss via a trait-mediated trophic cascade.

Although trophic cascades were originally believed to be driven only by predators eating prey, there is mounting evidence that such cascades can be generated in large part via non-consumptive effects. This is especially important in cascades affecting habitat-forming foundation species that in turn, influence associated communities. Here, we use laboratory and field experiments to identify a trait-mediated indirect interaction between predators and an abundant kelp in a marine temperate reef system. Predation risk from a microcarnivorous fish, the señorita, suppressed grazing by the host-specific seaweed limpet, which in turn, influenced frond loss of the habitat-forming feather boa kelp. This trophic cascade was pronounced because minor amounts of limpet grazing decreased the strength required to break kelp fronds. Cues from fish predators mitigated kelp loss by decreasing limpet grazing; we found 86% of this indirect interaction between predator and kelp was attributed to the non-consumptive effect in the laboratory and 56% when applying the same effect size calculations to the field. In field manipulations, the non-consumptive effect of señorita was as strong as the total predator effect and most importantly, as strong as the uncaged, "open" treatment with natural levels of predators. Our findings demonstrate that the mere presence of this fish reduces frond loss of the feather boa kelp through a trait-mediated trophic cascade. Moreover, despite large volumes of water, current flow, and wave energy, we clearly demonstrate a strong non-consumptive effect via an apparent chemical cue from señorita, suggesting that chemically mediated trait-driven cascades may be more prevalent in subtidal marine systems than we are currently aware.

Declines in plant palatability from polar to tropical latitudes depend on herbivore and plant identity.

Long-standing theory predicts that the intensity of consumer-prey interactions declines with increasing latitude, yet for plant-herbivore interactions, latitudinal changes in herbivory rates and plant palatability have received variable support. The topic is of growing interest given that lower-latitude species are moving poleward at an accelerating rate due to climate change, and predicting local interactions will depend partly on whether latitudinal gradients occur in these critical biotic interactions. Here, we assayed the palatability of 50 seaweeds collected from polar (Antarctica), temperate (northeastern Pacific; California), and tropical (central Pacific; Fiji) locations to two herbivores native to the tropical and subtropical Atlantic, the generalist crab Mithraculus sculptus and sea urchin Echinometra lucunter. Red seaweeds (Rhodophyta) of polar and temperate origin were more readily consumed by urchins than were tropical reds. The decline in palatability with decreasing latitude is explained by shifts in tissue organic content along with the quantity and quality of secondary metabolites, degree of calcification or both. We detected no latitudinal shift in palatability of red seaweeds to crabs, nor any latitudinal shifts in palatability of brown seaweeds (Phaeophyta) to either crabs or urchins. Our results suggest that evolutionary pressure from tropical herbivores favored red seaweeds with lower palatability, either through the production of greater levels of chemical defenses, calcification, or both. Moreover, our results tentatively suggest that the "tropicalization" of temperate habitats is facilitated by the migration of tropical herbivores into temperate areas dominated by weakly defended and more nutritious foods, and that the removal of these competing seaweeds may facilitate the invasion of better-defended tropical seaweeds.

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.

Season-specific impacts of climate change on canopy-forming seaweed communities.

Understory assemblages associated with canopy-forming species such as trees, kelps, and rockweeds should respond strongly to climate stressors due to strong canopy-understory interactions. Climate change can directly and indirectly modify these assemblages, particularly during more stressful seasons and climate scenarios. However, fully understanding the seasonal impacts of different climate conditions on canopy-reliant assemblages is difficult due to a continued emphasis on studying single-species responses to a single future climate scenario during a single season. To examine these emergent effects, we used mesocosm experiments to expose seaweed assemblages associated with the canopy-forming golden rockweed, Silvetia compressa, to elevated temperature and pCO2 conditions reflecting two projected greenhouse emission scenarios (RCP 2.6 [low] & RCP 4.5 [moderate]). Assemblages were grown in the presence and absence of Silvetia, and in two seasons. Relative to ambient conditions, predicted climate scenarios generally suppressed Silvetia biomass and photosynthetic efficiency. However, these effects varied seasonally-both future scenarios reduced Silvetia biomass in summer, but only the moderate scenario did so in winter. These reductions shifted the assemblage, with more extreme shifts occurring in summer. Contrarily, future scenarios did not shift assemblages within Silvetia Absent treatments, suggesting that climate primarily affected assemblages indirectly through changes in Silvetia. Mesocosm experiments were coupled with a field Silvetia removal experiment to simulate the effects of climate-mediated Silvetia loss on natural assemblages. Consistent with the mesocosm experiment, Silvetia loss resulted in season-specific assemblage shifts, with weaker effects observed in winter. Together, our study supports the hypotheses that climate-mediated changes to canopy-forming species can indirectly affect the associated assemblage, and that these effects vary seasonally. Such seasonality is important to consider as it may provide periods of recovery when conditions are less stressful, especially if we can reduce the severity of future climate scenarios.

Population responses of omnivorous arthropods to plant alternative resources suppress prey populations: A meta-analysis.

Omnivory is ubiquitous in ecological communities. Yet, we lack a consensus of how plant alternative resources impact the ability of omnivores to suppress prey populations. Previous work suggests that plant alternative resources can increase, decrease, or have no effect on the magnitude of omnivore-prey interactions. This discrepancy may arise from (1) the ability of omnivore populations to respond to plant alternative resources and (2) identity-specific effects of plant alternative resources. We used a meta-analysis to examine how omnivore population responses and the identity of plant alternative resources affect (1) omnivore predation rates (mainly reported as per capita predation rate) and (2) omnivore impacts on prey population density. Plant alternative resources reduced omnivore predation rate regardless of identity. The suppression of the predation rate by flowers and flowering plants was magnified when pollen alone was tested as the alternative resource. Surprisingly, plant alternative resource availability reduced prey density, suggesting that omnivore predation increased with plant alternative resources. This discrepancy (plant alternative resources not only decreased omnivore predation rates but also decreased prey density) resulted from experimental differences in the ability of omnivore populations to respond to plant alternative resources. In the presence of plant alternative resources, allowing omnivore population responses decreased prey density, while not allowing population responses increased prey density. Because omnivores commonly suppress prey density in the presence of plant alternative resources when population responses of omnivores are allowed, the effectiveness of biological control may depend upon the availability of such resources and the facilitation of population responses.

Aboveground competition influences density-dependent effects of cordgrass on sediment biogeochemistry.

Interspecific interactions between plants influence plant phenotype, distribution, abundance, and community structure. Each of these can, in turn, impact sediment biogeochemistry. Although the population and community level impacts of these interactions have been extensively studied, less is known about their effect on sediment biogeochemistry. This is surprising given that many plants are categorized as foundation species that exert strong control on community structure. In southern California salt marshes, we used clipping experiments to manipulate aboveground neighbor presence to study interactions between two dominant plants, Pacific cordgrass (Spartina foliosa) and perennial pickleweed (Sarcocornia pacifica). We also measured how changes in cordgrass stem density influenced sediment biogeochemistry. Pickleweed suppressed cordgrass stem density but had no effect on aboveground biomass. For every cordgrass stem lost per square meter, porewater ammonium increased 0.3-1.0 µM. Thus, aboveground competition with pickleweed weakened the effects of cordgrass on sediment biogeochemistry. Predictions about plant-soil feedbacks, especially under future climate scenarios, will be improved when plant-plant interactions are considered, particularly those containing dominant and foundation 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.

Local and regional variation in effects of burrowing crabs on plant community structure.

Burrowing animals can profoundly influence the structure of surrounding communities, as well as the performance of individual species. Changes in the community structure of burrowing animals or plants together with changing abiotic parameters could shift the influence of burrowers on surrounding habitats. For example, prior studies in salt marshes suggest that fiddler crabs stimulate cordgrass production, but leaf-grazing crabs suppress cordgrass production. Unfortunately, testing this prediction and others are impeded because few studies have examined crab impacts on the plant community and across multiple sites, multiple years, or both. This challenges our ability to predict how burrowing animals will influence plant community structure, and when and where these impacts will occur. We manipulated the densities of the dominant burrowing crabs in plant assemblages dominated by Pacific cordgrass (Spartina foliosa) and perennial pickleweed (Sarcocornia pacifica) at three sites in southern California for three years (2016, 2017, 2018). Crab impacts on plant community structure differed among each of our three sites. In contrast to our predictions, (1) leaf-grazing crabs (Pachygrapsus crassipes) had positive effects on cordgrass cover at one site and no effect on cordgrass production at a nearby site in the same marsh and (2) fiddler crabs (Uca crenulata) did not stimulate cordgrass production at another marsh. Because crabs affected traits of cordgrass, but not pickleweed, in the direction consistent with changes in cordgrass cover, we propose that marsh-specific crab effects on community structure were largely mediated through changes in cordgrass, as opposed to pickleweed. Importantly, crabs facilitated cordgrass during marsh-wide cordgrass loss, suggesting that crabs may mitigate environmental stress for this ecologically important plant. Because cordgrass abundance can be a critical measure of marsh functioning and is often a restoration target, we suggest that managing cordgrass populations would benefit from additional information about crab populations and their impacts among years, and among and within marshes.

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.

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).

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.

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.

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.

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 microm to large colonies of up to 30,000 microm 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.