Effect of a generalist mesopredator on modular and unitary sessile prey associated with a foundation species.

Unitary and modular sessile organisms both dominate in marine benthic communities, commonly preyed upon by the same generalist predators. The differences between unitary and modular defensive strategies may underlie the ways generalist predators control community structure, but this has never been empirically examined. We hypothesize that the individual size of an omnivorous mesopredatory shrimp affects the relative vulnerability of unitary and modular prey and hence translates into community structure. In a short-term laboratory microcosm experiment, we assessed the effect of the shrimp individual size on an epibiotic assemblage of red algae blades initially dominated by three species of modular bryozoans and a unitary serpulid tubeworm. We found that the individual size of a shrimp determines its effect on the prey community composition. Large shrimp stronger than small shrimp increased the proportion of unitary tubeworms among the epibionts surviving predation. While large shrimp reduced the proportions of all the three dominant bryozoan species, small shrimp, in contrast, mostly increased the proportion of a bryozoan species with the smallest modules and largest colonies. This bryozoan, like the tubeworms, demonstrated a higher survival rate with larger individual (colony) size. Yet, against large shrimp this bryozoan was outperformed by the largest tubeworms almost immune to predation. Partial predation by small shrimp modestly improved survival of the largest bryozoan colonies. Thus, relative vulnerability of unitary and modular prey is determined by the predator individual size. Our findings clarify the complex way the size structures of generalist consumers and their prey shape communities by affecting the species-specific relative performance of modular and unitary organisms. The demography of a foundation species and the competitive hierarchy can have additional effects by altering the balance of predation and competition.

Effects of a trophic cascade on a multi-level facilitation cascade.

The role of cascades in natural communities has been extensively studied, but interactions between trophic and facilitation cascades are unexplored. In the White Sea (65°N) shallow subtidal, bivalve primary facilitators provide hard substrate for secondary facilitator barnacles, that, in turn, provide substrate for conspecifics, ascidians, red algae and multiple associated organisms, composing a multi-level facilitation cascade. Previous research revealed that predation by the whelk Boreotrophon clathratus accounts for ~7% of adult barnacle mortality. Low whelk abundance limits their effect, with barnacles living on conspecifics several times more vulnerable to predation than those living on primary substrate. Trophic cascades can selectively shield foundation species from consumers, and hence may affect the structure and length of facilitation cascades. We tested the hypothesis that low abundance of the whelks results from mesopredator predation on their juveniles. Depending on the magnitude of the effect, this would mean that a trophic cascade controls the abundance of barnacles on all substrates or only barnacles living on conspecifics. We also suggested that barnacles on primary substrates and conspecifics facilitate different dependent assemblages. We manipulated the presence of crab and shrimp mesopredators in field caging experiments to assess their effect on whelk recruitment. In a field survey, we compared the assemblages of sessile macrobenthic organisms associated with barnacles living on different substrates. Caging experiments evidenced that crab and shrimp mesopredators reduce whelk recruitment by 4.6 times. Field data showed that barnacles on primary substrate and on conspecifics promote different dependent assemblages including secondary facilitator ascidians. Although mesopredators do not shield barnacles from elimination, their absence would restrict them from living on conspecifics. Barnacles on conspecifics are functionally different from barnacles on primary substrate, and can be considered a separate level of the facilitation cascade. Trophic cascades thus can generate community-wide effects on facilitation cascades by affecting their structure and possibly length.

Epibenthic predators control mobile macrofauna associated with a foundation species in a subarctic subtidal community.

Foundation species (FS) are strong facilitators providing habitat for numerous dependent organisms. The communities shaped by FS are commonly structured by interplay of facilitation and consumer control. Predators or grazers often indirectly determine community structure eliminating either FS or their principal competitors. Alternatively, they can prey on the dependent taxa directly, which is generally buffered by FS via forming complex habitats with numerous refuges. The latter case has been never investigated at high latitudes, where consumer control is widely considered weak. We manipulated the presence of common epibenthic crustacean predators to assess their effect on mobile macrofauna of the clusters developed by a FS (barnacle Balanus crenatus and its empty tests) in the White Sea shallow subtidal (65° N). While predation pressure on the FS itself here is low, the direct effects of a spider crab Hyas araneus and a shrimp Spirontocaris phippsii on the associated assemblages were unexpectedly strong. Removing the predators did not change species diversity, but tripled total abundance and altered multivariate community structure specifically increasing the numbers of amphipods, isopods (only affected by shrimp), and bivalves. Consumer control in the communities shaped by FS may not strictly follow the latitudinal predation gradient rule.

Cockles, barnacles and ascidians compose a subtidal facilitation cascade with multiple hierarchical levels of foundation species.

Facilitation cascades occur when multiple foundation species in a community are involved in a hierarchy of positive interactions, and consist of a primary facilitator which positively affects secondary facilitators, each supporting a suit of dependent species. There is no theoretical limit to the number of levels in a facilitation cascade, yet the existence of more than two has rarely been examined. We manipulated biogenic substrate produced by a primary facilitator (cockle shells) and a secondary facilitator (barnacles and their empty tests) in a space-limited subtidal community to test the hypothesis that solitary ascidians would be the third-level facilitator. In the field, most ascidians were found on barnacles, and most barnacles occupied cockle shells. To produce this pattern, barnacles could nurse ascidians (a longer 'facilitation chain') or outcompete them from cockle shells (a shorter chain). Experimental results clearly supported the nursing hypothesis providing evidence for a facilitation cascade with three hierarchical levels of foundation species. Our findings confirm that like predation and competition, positive interspecific interactions nest into multi-tier hierarchies with numerous levels. While the number of foundation species should increase community stability and resilience as it increases diversity and reduces environmental stress, facilitation chain length may have the opposite effect.

Bored to Death: Community-Wide Effect of Predation on a Foundation Species in a Low-Disturbance Arctic Subtidal System.

The strength of top-down control by consumers is predicted to decrease with latitude, but most data confirming this assumption come from latitudes <60°, while empirical studies of predation in sub-arctic and arctic marine habitats are few. A barnacle Balanus crenatus is a native foundation species in the shallow subtidal of the White Sea (65° N), hosting a diverse (250+ species) assemblage of macrobenthic organisms. On mixed sediments live barnacles share primary substrates (shells and gravel) with numerous empty barnacle tests, 7% of which had drill holes of an unidentified origin. We manipulated the densities of (i) adult muricid whelks Boreotrophon clathratus (of previously unknown feeding habits), to check if they prey on barnacles, (ii) other predators to reveal their effect on juvenile Boreotrophon, and (iii) empty tests to assess the community-wide effect of predation on barnacles. The abundance of drilled empty tests in the field correlated with that of Boreotrophon. A year-long caging experiment clearly confirmed predation, showing the highest barnacle mortality and proportion of drilled tests in whelk enclosures, and the lowest--in predator exclosure treatments. Boreotrophon preferred the barnacles attached to conspecifics to those from primary substrates. Because of its scarcity Boreotrophon had a minor direct effect on barnacle abundance in the field. Yet, initially defaunated empty tests and live barnacles developed markedly different macrobenthic assemblages, suggesting a strong indirect effect of the predation. Juvenile Boreotrophon were 5-6 times less abundant in open and partial cages than in exclosures and enclosures, which indicates that the recruitment and, consequently, the abundance of Boreotrophon and its predation on Balanus are top-down controlled by apex predators. In contrast, in tropical and temperate intertidal the predation on barnacles is stronger and primarily limited by environmental stress and prey availability.

Multiple foundation species shape benthic habitat islands.

Pattern generation by foundation species (FS) is a primary structuring agent in marine and terrestrial communities. Prior research, focused on single-species or guild-dominated habitats, stressed the role of facilitation in maintaining community structure. However, many habitats are developed by multiple FS from different guilds. Competition between these FS may provide an additional agent potentially responsible for spatial and temporal patterns. In the White Sea, epibenthic patches formed by barnacles (Balanus crenatus) and solitary ascidians (mainly Styela spp. and Molgula spp.) on small stones and empty bivalve shells (mainly Serripes groenlandicus) produce microhabitats for different sessile taxa. We hypothesized that: (1) several FS would provide habitats for most of other species in the community; (2) different FS promote different assemblages of sessile organisms; (3) the interplay of facilitation and competition best explains observed patterns of abundance and demography in FS; and (4) these interactions shape the whole community, increasing the diversity compared to less heterogeneous patches constituted by single FS. We examined 459 patches and the results generally supported this hypothesis. The number of FS in a patch positively affected species diversity. Most sessile species (72% of individuals) resided on barnacles, ascidians and red algae, except barnacles that dominated the primary substrate. The size structure of barnacles (live individuals and empty shells) and ascidians were interrelated, suggesting long-term patch dynamics whereby ascidians regularly replace barnacles. Following this replacement, we expect consequent changes to the entire dependent assemblage. Evidence for these changes exists in the spatial pattern: most sessile and motile taxa demonstrated significant associations with either FS. Our results indicate that the small-scale patterns observed in patches formed by multiple FS are primarily generated by facilitation of dependent taxa by FS, and facilitation and competition between different FS.