Carlos Robles

Responses of a Key Intertidal Predator to Varying Recruitment of Its Prey

How a predator responds to fluctuating prey abundances determines its capacity to regulate the preys population levels. Unlike many terrestrial and a few marine arthropods, key intertidal invertebrate predators, e.g., sea stars and whelks, have been portrayed as lacking rapid behavioral responses that would permit them to control episodes of massive prey recruitment. Our field experiments demonstrated that intertidal sea stars, Pisaster ochraceus, rapidly change densities and alter diet in response to varying recruitment of their prey, the mussels Mytilus spp. Densities of Pisaster foraging at high tide were positively correlated with an index of recruitment of Mytilus californianus. The sea stars aggregated in episodes of massive mussels recruitment and dispersed as local abundances of juveniles mussels declined. Aggregation and dispersal were reproduced in field experiments by adding or removing masses of 1st—yr Mytilus spp. to naturally occurring mussel beds. Over the 7 yr of the study, the lower margins of the mussel beds, a distributional limit set at least in some circumstances by the sea stars, remained relatively constant, despite significant year—to—year variation in mussel recruitment rates. We speculate that aggregation acts in concert with previously hypothesized long—term responses to stabilize the lower distributional limits of the mussels.

HISTORY AND CURRENT DEVELOPMENT OF A PARADIGM OF PREDATION IN ROCKY INTERTIDAL COMMUNITIES

A paradigm is a set of mutually supportive hypotheses that provides a frame of reference within a field. In 1962, Kuhn proposed that paradigms form within the dual contexts of empirical evidence and intellectual history. Facts potentially contradictory to a paradigm may not be recognized until they are observed repeatedly and incorporated as supportive evidence into a new theory. Support for this interpretation can be found in the history of a paradigm of predation in rocky intertidal communities. Hypotheses were developed in the contexts of innovative field experiments and historical arguments of competition theory. The resulting paradigm proposed that predators restrict populations of competitively dominant prey to refuges. Different types of refuge, or no refuge, prevail in different areas of the intertidal zone, accounting for patterns of prey distribution, the coexistence of natural enemies, and the local maintenance of diversity. An ensuing period of criticism made reference to potential contradictions. Rather than by predation alone, prey abundances are determined largely by an interplay of varying rates of predation and prey production. Furthermore, prey refuges are neither necessary nor sufficient to explain all observed instances of local coexistence of predators and prey. We present a model in which intertidal boundaries of prey are set by equilibria between predation and prey production. Predation and prey productivity vary with environmental gradients and with explicit spatial configurations of the prey. This synthesis relies on insights of the original paradigm, incorporates the contradictory observations, and depends on novel capabilities afforded by spatially explicit computer simulations. The resulting synthesis provides explanations for distinctive aspects of zonation, including abrupt prey boundaries in continuous gradients of predation, and converging upper and lower prey boundaries in gradients of decreasing wave exposure.

Influence of Biotic Factors in an Upper Intertidal Community: Dipteran Larvae Grazing on Algae

Field experiments were used to determine the effects of herbivorous fly larvae on ephemeral algae at several rocky beaches in central California. The larvae of marine Diptera form dense populations during seasonal blooms of ephemeral algae in certain higher areas of rocky shores. In three field experiments, changes in the percent cover and species composition of algae on natural and artificial substrates which larvae were allowed to colonize were compared with the changes in algal cover on otherwise similar substrates from which larvae were removed. A system of barriers constructed of copper paint, plastic, iron, and other materials was used to exclude grazing crabs and limpets, which otherwise might have confounded effects produced by the smaller Diptera larvae. In two unreplicated experiments, larval removals caused increases in algal abundance. Statistical analysis of a third, replicated, experiment showed that in certain circumstances the larvae changed the species composition of algal blooms. This effect apparently occurred when grazing hastened species replacements during algal succession. Grazing dipteran larvae are apparently part of a complex association of herbivores that influence algal succession and partially determine the abundances of some high intertidal algae.

CHANGING RECRUITMENT IN CONSTANT SPECIES ASSEMBLAGES: IMPLICATIONS FOR PREDATION THEORY IN INTERTIDAL COMMUNITIES

Ecological theory for benthic communities emphasizes intense species interactions that depend on the high productivity of sedentary invertebrates. The keystone predator hypothesis maintains that intense predation by one consumer species is necessary to prevent a prolific, competitively dominant prey species from eliminating other species using the same resource. This study considers the consequences of extreme spatial and temporal variation in the recruitment of a prey species supporting keystone and diffuse predation. Prior experiments on rocky shores of Santa Catalina Island, California, USA, demonstrated that predation by spiny lobsters (Panulirus interruptus) maintained a distinctive red algal turf by killing juvenile mussels (Mytilus californianus and M. galloprovincialis) that otherwise overgrow and replace the algae. In the present study, long-term surveys revealed that high recruitment of the predominant mussel, M. californianus, occurred only on the most wave-exposed sites in certain years; mussel recruitment was slight to nil on relatively protected sites in most years. A predator exclosure experiment consisting of seven replicates placed along the gradient of wave exposure demonstrated that the effects of predation depended upon the spatial differences in recruitment rates. Lobsters on wave-exposed sites functioned as keystone predators; on more sheltered sites, little or no predation, whether by lobsters or the fishes and whelks also foraging on the sheltered sites, was necessary to maintain the algal assemblage. Similar species assemblages can be maintained by markedly different relative levels of crucial ecological rates. In the mid-intertidal zone of Santa Catalina Island, the intense species interactions depicted in the keystone predator hypothesis occurred only at productive, high wave exposure locations; low recruitment of mussels elsewhere preempts both predation and the competition between the mussel and algal assemblages. Thus, red algae dominates rocky shores through different mechanisms over a range of physical conditions. The occurrences of low mussel recruitment do not appear to be anomalies, but rather a consequence of the life history of Mytilus californianus.

Varied carnivore effects and the prevalence of intertidal algal turfs

Abstract A red algal turf covers mid-shore levels of much of the California Channel Islands. Our experiments at Santa Catalina Island show that carnivores maintain the turf by consuming juvenile mussels Mytilus spp. and associated invertebrates. Exclusion of spiny lobsters Panulirus interruptus (Randall) from comparatively wave-exposed sites caused the complete and persistent replacement of the turf by the mussel assemblage. On sites protected from wave action, the lobsters were joined by carnivorous fishes, i.e., Halichoeres semisinctus (Ayrcs), Oxyjulis californica (Gunther) and Semicossyphus pulcher (Ayres), and whelks, i.e., Ceratostoma nuttalli (Conrad) and Maxwellia gemma (Sowerby). Compensatory foraging shifts by the whelks prevented significant increases of mussels in lobster and fish exclosures. Exclusion of all predators at the protected site caused a moderate but statistically significant increase. Thus, experiments at different sites indicated either “keystone” or “diffuse” effects of predators. Experimental clumps of large Mytilus californianus (Conrad) persisted longer after re-exposure to predation in the post-experimental periods than did clumps of smaller M. Californianus or M. edulis L. Transplants of matched cohorts indicated that the size differences of mussels in the exclosure experiments were caused by differences in shell growth rates correlated with wave exposure. We speculate that changing growth rates may influence the outcome of size-limited predation, accounting for some of the variation in the relative abundance of turf and mussels over the wave exposure gradient.

Effect of Algal Epiphytes on the Mussel Mytilus Californianus

The effects of facultative epiphytes on a bivalve host were studied on an islet near Santa Catalina Island, California. The primary cover in the mid-intertidal zone was a mosaic of red algal turf (Corallina officinalis, Gigartina canaliculata, and Gelidium coulteri) and clumps of the mussel Mytilus californianus. In certain circumstances the algae attached to and overgrew the mussels. In other marine habitats, facultative epibionts benefit bivalve hosts by masking them from predators. At Catalina, spiny lobsters (Panulirus interruptus) and oystercatchers (Hae- matopus bachmani) preyed on intertidal mussels. However, in tagging studies, overgrown mussels displayed a nonsignificant trend towards lower survivorship. A factorial experiment manipulating exposure to predators and the cover of epiphytes demonstrated that over- growth significantly reduced survivorship. There was no significant statistical interaction between treatment effects, indicating that the presence of algae did not protect the mussels from predators. Overgrown mussels also had significantly lower rates of growth and re- production than naturally clear mussels of similar size and location. Experimental removal of the epiphytes caused significant increases in mussel growth and reproduction relative to overgrown controls. In the community circumstances chosen for this study, the epiphytic habit is a part of the processes in which otherwise freeliving algae become dominant on the rock surface.

Diel variation of intertidal foraging by Cancer productus L. in British Columbia

Scuba was used at high tide to observe the foraging activity of Cancer Productus L. on the rocky shores of British Columbia. Intertidal foraging occurred most frequently on shores protected from wave action. In the latter areas crabs displayed marked diel shifts in density, size, and sex ratio. Crabs did not forage intertidally at low water, but increased from 0·015 m-2 to 0·15 m-2 between day and night high tides. Day foraging crabs were predominantly males (86%) and significantly larger than night foraging crabs of either sex. Females were more common (64%) in the night. Juveniles and mating pairs occurred in the intertidal zone only on nocturnal high tides. Size/sex differences in movement patterns appear to be an important feature of the life histories of some cancrid crabs.

Disturbance and predation in an assemblage of herbivorous Diptera and algae on rocky shores

SummarySpeculation about the effects of disturbance in marine benthic communities is often based on competition theory. Disturbances are thought to “provision” numerically depleted or competitively inferior species with resources associated with open substrate. However, disturbances that remove entire assemblages of sessile species also alter trophic structure, and thereby, influence the outcome of predator/prey relations. Aspects of community structure may be determined by patterns of disturbance and predation.The influence of disturbance and predation on the distribution and seasonality of blooms of ephemeral algae and associated Diptera was investigated with field experiments at several rocky beaches in central California. Blooms of ephemeral algae developed on high intertidal rock faces that were subject to severe seasonal disturbances caused by shifting sediment. These were subsequently colonized by the herbivorous larvae of several Diptera species for predictable periods each year. Other areas, without blooms, were not so disturbed.Experiments were done to determine if seasonal blooms were caused by seasonal disturbances that remove predators which otherwise might prevent the establishment of the Diptera/algae assemblage. The predators were crabs and limpets which eat both algae and larvae while foraging. Blooms of algae and larvae did not develop when limpets were transplanted to disturbed areas in periods between disturbances. Adjacent control areas did support blooms. Transplanted limpets did not survive periods of burial. When both limpets and crabs were excluded from treatment plots in undisturbed areas, blooms developed where they would not otherwise have occurred; controls remaied unchanged. Crabs and limpets differed in their effects on this assemblage. Crabs recruited quickly to the site of a bloom, but did not crop algal cover as closely, nor decrease larval density as much as the slowly recruiting limpets.The results suggest that disturbances favor blooms of some species by reducing predation. Severe localized disturbances increased the variability of the upper shore community by creating a patchwork of differing predator/prey abundances.

Complex equilibria in the maintenance of boundaries: experiments with mussel beds

Stationary boundaries of sedentary species may belie dynamic processes that form them. Our aim was to test an implication of an evolving body of theory, that such boundaries are manifestations of complex regulatory dynamics. On rocky shores of British Columbia, large-scale field experiments altered the densities of predatory sea stars (Pisaster ochraceus), causing shifts in the location of the lower vertical boundaries of their prey, sea mussels (Mytilus californianus). While control mussel beds remained unchanged, experimental reductions of sea star densities caused the downward extension of the lower boundaries, and experimental increases in sea stars densities caused the upward recession of the lower boundary well into the zone presumed to be a spatial refuge from predation. Cleared plots prepared within the initial boundaries were recolonized to varying degrees, depending on predator densities. After 30 months, plots on sea star removal sites showed high densities of adult mussels, control plots showed intermediate densities, and sea star addition plots showed only a sparse cover of alternative prey. Observations by divers at high tide showed that as small prey were depleted progressively from removal, to control, to addition sites, correspondingly larger mussels were attacked, including very large individuals comprising the lower boundary of addition sites. The findings contradict classic theory of zonation based on static prey refuges and support an alternative theory in which boundaries are maintained by complex, spatially structured equilibria.

Mussel Bed Boundaries as Dynamic Equilibria: Thresholds, Phase Shifts, and Alternative States

Ecological thresholds are manifested as a sudden shift in state of community composition. Recent reviews emphasize the distinction between thresholds due to phase shifts—a shift in the location of an equilibrium—and those due to alternative states—a switch between two equilibria. Here, we consider the boundary of intertidal mussel beds as an ecological threshold and demonstrate that both types of thresholds may exist simultaneously and in close proximity on the landscape. The discrete lower boundary of intertidal mussel beds was long considered a fixed spatial refuge from sea star predators; that is, the upper limit of sea star predation, determined by desiccation tolerance, fixed the lower boundary of the mussel bed. However, recent field experiments have revealed the operation of equilibrium processes that maintain the vertical position of these boundaries. Here, we cast analytical and simulation models in a landscape framework to show how the discrete lower boundary of the mussel bed is a dynamic predator-prey equilibrium, how the character of that boundary depends on its location in the landscape, and how boundary formation is robust to the scale of local interactions.