Bruce A. Menge

Challenges in the quest for keystones

Mary E. Power is a professor in the Department of Integrative Biology, University of California, Berkeley, CA 94720. David Tilman is a professor in the Department of Ecology, Evolution, and Behavior, University of Minnesota, St. Paul, MN 55108. James A. Estes is a wildlife biologist in the National Biological Service, Institute of Marine Science, University of California, Santa Cruz, CA 95064. Bruce A. Menge is a professor in the Department of Zoology, Oregon State University, Corvallis, OR 97331. William J. Bond is a professor doctor in the Department of Botany, University of Cape Town, Rondebosch 7700 South Africa. L. Scott Mills is an assistant professor in the Wildlife Biology Program, School of Forestry, University of Montana, Missoula, MT 59812. Gretchen Daily is Bing Interdisciplinary Research Scientist, Department of Biological Science, Stanford University, Stanford, CA 94305. Juan Carlos Castilla is a full professor and marine biology head in Facultad de Ciencias Biologicas, Pontificia Universidad Catolica de Chile, Casilla 114-D, Santiago, Chile. Jane Lubchenco is a distinguished professor in the Department of Zoology, Oregon State University, Corvallis, OR 97331. Robert T. Paine is a professor in the Department of Zoology, NJ-15, University of Washington, Seattle, WA 98195. ? 1996 American Institute of Biological Sciences. A keystone species is

Community Regulation: Variation in Disturbance, Competition, and Predation in Relation to Environmental Stress and Recruitment

We present a model of community regulation that incorporates the effects of abiotic disturbance, predation, competition, and recruitment density. We assume that mobile organisms (i.e., consumers) are more strongly affected by environmental stress than are sessile organisms and that food-web complexity decreases with increasing stress. The model makes three predictions under conditions of high recruitment. First, in stressful environments, consumers have no effect because they are absent or inactive, and competition for space is prevented. Both mobile and sessile organisms are regulated directly by environmental stress. Second, in moderate environments, consumers are still ineffective, but sessile organisms are less affected by stress and frequently attain high densities, leading to competition for space. Finally, in benign environments, consumers prevent competition for space unless the prey can escape a predation bottleneck and reach a high abundance. A reduction in recruitment density reduces the importance of competition for a given level of environmental stress. At top trophic levels, low recruitment slows the rate of population increase, and competition should be less intense even in benign environments. In stressful environments, severe conditions should keep the density of consumers low regardless of recruitment density. Abiotic stress should regulate mobile consumers over a wider range of the environmental gradient with low rather than with high recruitment. At low trophic levels, the importance of competition (including escape competition) should decline with reduced recruitment density regardless of the level of stress. With low recruitment, lower trophic levels should be regulated by physical factors at the severe end of the environmental gradient and by predation at the benign end of the gradient. This model also predicts that when competition for space leads to exclusion and recruitment is high, the relationships between diversity and either predation (the predation hypothesis) or disturbance (the intermediate-disturbance hypothesis) are distinct, not equivalent as is often assumed. We suggest that physical disturbance is distinct from predation (considered equivalent to, but distinct from, biological disturbance). Diversity is low in harsh environments because of the intolerance of all but opportunistic and highly resistant species to such conditions. With environmental moderation, diversity increases because of the intermediate-disturbance effect, decreases because of the competitive-exclusion effect, increases because of the prevention of competitive exclusion by moderate predation, and decreases because of the local extinction of prey by severe predation. Thus, with high recruitment, a bimodal diversity curve is predicted along the axis of environmental stress. If competition permits coexistence or recruitment is low, the diversity curve is predicted to be unimodal. The model should be applicable in all habitats, although some predictions may be altered by differences in the importance of omnivory in terrestrial versus aquatic interaction webs. Testing the model will be difficult, but it is feasible; it will require quantification of local environmental gradients, recruitment densities, food-web structure, and spatial structure. Predictions can be made on the basis of these observations and tested by the determination of community organization using experiments that simultaneously evaluate the effects of the major processes structuring the community. Partial tests from marine habitats support some predictions of the model, but further testing is needed, particularly in nonmarine habitats.

The Keystone Species Concept: Variation in Interaction Strength in a Rocky Intertidal Habitat

The usefulness and generality of the keystone species concept has recently been questioned. We investigated variation in interaction strength between the original keystone predator, the seastar Pisaster ochraceus, and its primary prey, mussels (Mytilus californianus and M. trossulus). The study was prompted by differences in community structure at two low zone sites along the central Oregon coast, Boiler Bay (BB) and Strawberry Hill (SH). Predators, especially seastars, were larger and more abundant at SH than at BB. Further, sessile animals were more abundant and macrophytes were less abundant at SH. Predators were more abundant at wave—exposed sites at both sites, and at SH, sessile invertebrates were more abundant at the wave—exposed location and sand cover was high at the wave—protected location. To test the hypothesis that variation in predation strength explained some of these differences, we examined the seastar—mussel interaction at locations with high and low wave exposure at both sites. Predation intensity was quantified by determining the survival of mussels in clumps (50 mussels per clump, shell length 4—7 cm) transplanted to large plots (18—163 m2) with or without seastars in the low intertidal zone. Predation effects were quantified by determining prey recolonization rates in marked quadrats in the same large plots. Spatial variation in interaction strength was quantified by examining predation at scales of metres (among transplants within plots), 10s of metres (between replicate plots within each exposure at each site), 100s of metres (between wave exposures within locations), and 10 000s of metres (between sites). Temporal variation was evaluated by performing the experiments in 1990 and 1991. The relation between prey (mussel) recruitment and growth to differences in community structure was evaluated by quantifying recruitment density in plastic mesh balls (collectors) and growth of individually marked transplanted mussels, respectively, at each site ° exposure ° tide level combination each month for 4 yr. Predation intensity varied greatly at all spatial scales. At the two largest spatial scales (10s of kilometres, 100s of metres), differences in both survival of transplanted mussels and prey recolonization depended on variation in seastar abundance with site, wave exposure, prey recruitment and growth, and at SH protected, the extent of sand burial. Variation at the two smallest scales (metres, 10s of metres) was high when seastars were scarce and low when seastars were abundant. Transplanted mussels suffered 100% mortality in 2 wk at wave—exposed SH, but took >52 wk at wave—protected BB. Seastar effects on prey recolonization were detected only at the SH wave—exposed site. Here, where prey recruitment and growth were unusually high, the mussel M. trossulus invaded and dominated space within 9 mo. After 14 mo, whelks, which increased in both size and abundance in the absence of Pisaster, arrested this increase in mussel abundance. Similar changes did not occur at other site ° exposure combinations, evidently because prey recruitment was low and possibly also due to whelk predation on juveniles. Longer term results indicate that, as in Washington state, seastars prevent large adult M. californianus from invading lower intertidal regions, but only at wave—exposed, not wave—protected sites. Thus, three distinct predation regimes were observed: (1) strong keystone predation by seastars at wave—exposed headlands; (2) less—strong diffuse predation by seastars, whelks, and possibly other predators at a wave—protected cove, and (3) weak predation at a wave—protected site buried regularly by sand. Comparable experimental results at four wave—exposed headlands (our two in Oregon and two others in Washington), and similarities between these and communities on other West Coast headlands suggest keystone predation occurs broadly in this system. Results in wave—protected habitats, however, suggest it is not universal. In Oregon, keystone predation was evidently contingent on conditions of high prey production (i.e., recruitment and growth), while diffuse predation occurred when prey production was low, and weak predation occurred when environmental stress was high. Combining our results with examples from other marine and non—marine habitats suggests a need to consider a broader range of models than just keystone predation. The predictive and explanatory value of an expanded set of models depends on identifying factors distinguishing them. Although evidence is limited, a survey of 17 examples suggests (1) keystone predation is evidently not distinguished from diffuse predation by any of 11 previously proposed differences, but (2) may be distinguished by rates of prey production. Further, (3) differential predation on competitively dominant prey does not distinguish keystone from nonkeystone systems, since this interaction occurs in both types of community. Instead, differential predation on dominant prey evidently distinguishes strong—from weak—predation communities. While the keystone predation concept has been and will continue to be useful, a broadened focus on testing and developing more general models of community regulation is needed.

Role of scale and environmental factors in regulation of community structure

Pattern in ecological communities - the distribution, abundance and diversity of species - depends on a complex interplay between large - and local-scale processes. Large-scale variation in factors such as environmental stress, dispersal or productivity sets the stage for local-scale ecological processes such as predation or competition. Until recently, most research focused on local-scale explanations of community pattern. Current models attempt to integrate the role of individual large-scale factors with local-scale processes. This trend will continue, with increased effort to understand the specific means by which large-scale factors cause variation among communities.

Emergence of Anoxia in the California Current Large Marine Ecosystem

Eastern boundary current systems are among the worlds most productive large marine ecosystems. Because upwelling currents transport nutrient-rich but oxygen-depleted water onto shallow seas, large expanses of productive continental shelves can be vulnerable to the risk of extreme low-oxygen events. Here, we report the novel rise of water-column shelf anoxia in the northern California Current system, a large marine ecosystem with no previous record of such extreme oxygen deficits. The expansion of anoxia highlights the potential for rapid and discontinuous ecosystem change in productive coastal systems that sustain a major portion of the worlds fisheries.

Upwelling-driven nearshore hypoxia signals ecosystem and oceanographic changes in the northeast Pacific.

Seasonal development of dissolved-oxygen deficits (hypoxia) represents an acute system-level perturbation to ecological dynamics and fishery sustainability in coastal ecosystems around the globe. Whereas anthropogenic nutrient loading has increased the frequency and severity of hypoxia in estuaries and semi-enclosed seas, the occurrence of hypoxia in open-coast upwelling systems reflects ocean conditions that control the delivery of oxygen-poor and nutrient-rich deep water onto continental shelves. Upwelling systems support a large proportion of the worlds fisheries, therefore understanding the links between changes in ocean climate, upwelling-driven hypoxia and ecological perturbations is critical. Here we report on the unprecedented development of severe inner-shelf (<70 m) hypoxia and resultant mass die-offs of fish and invertebrates within the California Current System. In 2002, cross-shelf transects revealed the development of abnormally low dissolved-oxygen levels as a response to anomalously strong flow of subarctic water into the California Current System. Our findings highlight the sensitivity of inner-shelf ecosystems to variation in ocean conditions, and the potential impacts of climate change on marine communities.

Community Organization in Temperate and Tropical Rocky Intertidal Habitats: Prey Refuges in Relation to Consumer Pressure Gradients

The structure of a tropical rocky intertidal community on Taboguilla Island on the Pacific coast of Panama is characterized by extremely low abundances of noncrustose algae and sessile animals, indistinct vertical zonation patterns (a result of the low abundances), and the occurrence of most invertebrates (except barnacles) and upright algae in holes and crevices (as opposed to open, smooth surfaces). This contrasts strikingly with two temperate rocky intertidal communities, which have high covers of plants and animals, more obvious zones, and invertebrates and upright algae occurring both on relatively homogeneous surfaces and in holes and crevices. Field experiments were done and observations were made in the Panama community to test the effects of different types of consumers (both predators and herbivores) on their prey and on the types of escapes utilized by the prey. Consumer exclusion experiments suggest that (1) predation and herbivory are severe at all times of the year, (2) consumer pressure is a cumulative function of many types and species of predators and herbivores, (3) the primary effect of larger fishes and crabs is to restrict most prey to three—dimensional refuges (holes and crevices), and (4) the primary effect of smaller consumers, mostly invertebrates, is to keep abundances of the prey low. Thus, in the Panama system, three—dimensional space (holes and crevices) appears to be particularly important as a refuge from consumers, while escapes from consumers in body size, time, or two—dimensional space (e.g., in a higher zone) documented so frequently in temperate areas, assume secondary importance for many prey. This restriction of the types of escapes utilized by prey species appears to be a consequence of two main factors: the presence of fast—moving consumers (i.e., herbivorous and predaceous fishes and herbivorous crabs which are absent or rare in the two temperate communities), and the year—round foraging of all consumers.

Delayed upwelling alters nearshore coastal ocean ecosystems in the northern California current

Wind-driven coastal ocean upwelling supplies nutrients to the euphotic zone near the coast. Nutrients fuel the growth of phytoplankton, the base of a very productive coastal marine ecosystem [Pauly D, Christensen V (1995) Nature 374:255–257]. Because nutrient supply and phytoplankton biomass in shelf waters are highly sensitive to variation in upwelling-driven circulation, shifts in the timing and strength of upwelling may alter basic nutrient and carbon fluxes through marine food webs. We show how a 1-month delay in the 2005 spring transition to upwelling-favorable wind stress in the northern California Current Large Marine Ecosystem resulted in numerous anomalies: warm water, low nutrient levels, low primary productivity, and an unprecedented low recruitment of rocky intertidal organisms. The delay was associated with 20- to 40-day wind oscillations accompanying a southward shift of the jet stream. Early in the upwelling season (May–July) off Oregon, the cumulative upwelling-favorable wind stress was the lowest in 20 years, nearshore surface waters averaged 2°C warmer than normal, surf-zone chlorophyll-a and nutrients were 50% and 30% less than normal, respectively, and densities of recruits of mussels and barnacles were reduced by 83% and 66%, respectively. Delayed early-season upwelling and stronger late-season upwelling are consistent with predictions of the influence of global warming on coastal upwelling regions.

A LATITUDINAL GRADIENT IN RECRUITMENT OF INTERTIDAL INVERTEBRATES IN THE NORTHEAST PACIFIC OCEAN

A latitudinal gradient in the recruitment rates of intertidal mussels and barnacles was detected in the Northeast Pacific during 1996 and 1997. This gradient was approximately a stepcline: annual recruitment, on average, was 1-2 orders of magnitude higher in central and northern Oregon than in central and northern California. In contrast to the regional differences, large-scale gradients in recruitment within California were small: correlations of recruitment with latitude were weak, and, in all but one case, statistically insignificant. Nonetheless, trends in the data suggest that recruitment within central and northern California was highest between San Francisco and Monterey Bay, where larvae may be retained more nearshore than to the north or south. If so, apparently conflicting claims about latitudinal gradients in recruitment within California can be reconciled. The large scale transition in recruitment rates supports the hypothesis that a marked shift in the intensity of upwelling near Cape Blanco in southern Oregon is a major cause of a coincident transition in community structure. Stronger upwelling (and thus offshore flow) to the south has been hypothesized to transport larvae further offshore and thereby reduce larval supply to nearshore benthic communities. This study confirms that the predicted differences in recruitment exist, and that these differences are large. Preliminary calculations indicate that regional differences in offshore flow are likely to make a larger contribution to the recruitment transitions than several other plausible causes. In addition, recruitment transitions are larger, more abrupt, and more consistent across species than corresponding shifts in percentage cover, which favor competitive dominants. This supports model predictions that competition for space is more intense where recruitment is high. However, the absence of strong, large-scale recruitment gradients within California suggests that mesoscale processes are relatively more important than latitudinal trends in upwelling as determinants of community structure patterns at smaller scales.

Predation intensity in a rocky intertidal community

SummaryKnowledge of predation intensity and how and why it varies among communities appears to be a key to understanding of community regulation. Along the rocky shores of New England, predation intensity in the mid intertidal zone appears to be low with exposure to severe wave shock, low desiccation stress, and a sparse cover of canopy algae, and high at areas protected from waves, with high desiccation potential and a dense cover of algae. As a result, predators at exposed headlands have no controlling influence on community structure, while at protected sites, they exert a strong and controlling effect on community structure.Experimental-observational studies of the effects of wave shock and desiccation on survival, foraging range and activity of the primary predator in this community (Thais lapillus) indicate that:(1)wave shock is a continuous and actual source of mortality at exposed sites but is relatively unimportant at protected sites;(2)mortality rates from desiccation at protected sites are potentially high and greater than at exposed sites; however,(3)actual desiccation stress is greatly reduced at protected sites by a dense algal canopy;(4)mortality from desiccation is greater in the higher mid intertidal than in the lower mid intertidal. Comparisons of activity patterns of Thais from April through November (these snails are usually active from May to early October) at an exposed and a protected site suggest snails at the former site restrict their active feeding to crevices while those at the latter site forage throughout the habitat. Field experiments support this hypothesis. Hence, differences in predator effectiveness at exposed and protected communities are probably due in part to the influence of wave shock. Exposed areas receive frequent severe wave shock in all seasons, even summer. Thus, the risk of being swept off the shore for snails foraging away from the shelter of a crevice at such areas is apparently great and exerts a strong selective force on foraging range. The importance of waves as a selective agent is further reinforced by the fact that crevices are nearly barren of prey, while just a few cm beyond the limits of the crevice, prey occur in great abundance.In contrast, at protected sites wave shock is never as severe as at exposed sites and is a relatively minor factor among several which might affect the foraging activity of a Thais. A major factor which varies among protected sites is the algal canopy. The influence of this factor is considered in a companion paper.