Eric L. Berlow

Approaching a state shift in Earth’s biosphere

Localized ecological systems are known to shift abruptly and irreversibly from one state to another when they are forced across critical thresholds. Here we review evidence that the global ecosystem as a whole can react in the same way and is approaching a planetary-scale critical transition as a result of human influence. The plausibility of a planetary-scale ‘tipping point’ highlights the need to improve biological forecasting by detecting early warning signs of critical transitions on global as well as local scales, and by detecting feedbacks that promote such transitions. It is also necessary to address root causes of how humans are forcing biological changes.

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.

Two degrees of separation in complex food webs

Feeding relationships can cause invasions, extirpations, and population fluctuations of a species to dramatically affect other species within a variety of natural habitats. Empirical evidence suggests that such strong effects rarely propagate through food webs more than three links away from the initial perturbation. However, the size of these spheres of potential influence within complex communities is generally unknown. Here, we show for that species within large communities from a variety of aquatic and terrestrial ecosystems are on average two links apart, with >95% of species typically within three links of each other. Species are drawn even closer as network complexity and, more unexpectedly, species richness increase. Our findings are based on seven of the largest and most complex food webs available as well as a food-web model that extends the generality of the empirical results. These results indicate that the dynamics of species within ecosystems may be more highly interconnected and that biodiversity loss and species invasions may affect more species than previously thought.

More than a meal… integrating non‐feeding interactions into food webs

Organisms eating each other are only one of many types of well documented and important interactions among species. Other such types include habitat modification, predator interference and facilitation. However, ecological network research has been typically limited to either pure food webs or to networks of only a few (<3) interaction types. The great diversity of non-trophic interactions observed in nature has been poorly addressed by ecologists and largely excluded from network theory. Herein, we propose a conceptual framework that organises this diversity into three main functional classes defined by how they modify specific parameters in a dynamic food web model. This approach provides a path forward for incorporating non-trophic interactions in traditional food web models and offers a new perspective on tackling ecological complexity that should stimulate both theoretical and empirical approaches to understanding the patterns and dynamics of diverse species interactions in nature.

Foraging theory predicts predator-prey energy fluxes

1. In natural communities, populations are linked by feeding interactions that make up complex food webs. The stability of these complex networks is critically dependent on the distribution of energy fluxes across these feeding links. 2. In laboratory experiments with predatory beetles and spiders, we studied the allometric scaling (body-mass dependence) of metabolism and per capita consumption at the level of predator individuals and per link energy fluxes at the level of feeding links. 3. Despite clear power-law scaling of the metabolic and per capita consumption rates with predator body mass, the per link predation rates on individual prey followed hump-shaped relationships with the predator-prey body mass ratios. These results contrast with the current metabolic paradigm, and find better support in foraging theory. 4. This suggests that per link energy fluxes from prey populations to predator individuals peak at intermediate body mass ratios, and total energy fluxes from prey to predator populations decrease monotonically with predator and prey mass. Surprisingly, contrary to predictions of metabolic models, this suggests that for any prey species, the per link and total energy fluxes to its largest predators are smaller than those to predators of intermediate body size. 5. An integration of metabolic and foraging theory may enable a quantitative and predictive understanding of energy flux distributions in natural food webs.

PREDATOR DIVERSITY AND IDENTITY DRIVE INTERACTION STRENGTH AND TROPHIC CASCADES IN A FOOD WEB

Declining predator diversity may drastically affect the biomass and productivity of herbivores and plants. Understanding how changes in predator diversity can propagate through food webs to alter ecosystem function is one of the most challenging ecological research topics today. We studied the effects of predator removal in a simple natural food web in the Sierra Nevada mountains of California (USA). By excluding the predators of the third trophic level of a food web in a full-factorial design, we monitored cascading effects of varying predator diversity and composition on the herbivorous beetle Chrysomela aeneicollis and the willow Salix orestera, which compose the first and second trophic levels of the food web. Decreasing predator diversity increased herbivore biomass and survivorship, and consequently increased the amount of plant biomass consumed via a trophic cascade. Despite this simple linear mean effect of diversity on the strength of the trophic cascade, we found additivity, compensation, and interference in the effects of multiple predators on herbivores and plants. Herbivore survivorship and predator-prey interaction strengths varied with predator diversity, predator identity, and the identity of coexisting predators. Additive effects of predators on herbivores and plants may have been driven by temporal niche separation, whereas compensatory effects and interference occurred among predators with a similar phenology. Together, these results suggest that while the general trends of diversity effects may appear linear and additive, other information about species identity was required to predict the effects of removing individual predators. In a community that is not temporally well-mixed, predator traits such as phenology may help predict impacts of species loss on other species. Information about predator natural history and food web structure may help explain variation in predator diversity effects on trophic cascades and ecosystem function.

SHRUB EXPANSION IN MONTANE MEADOWS: THE INTERACTION OF LOCAL‐SCALE DISTURBANCE AND SITE ARIDITY

Montane meadows in the Sierra Nevada of California have experienced dra- matic expansion of shrubs (Artemisia rothrockii) and reduction in herbaceous species cover since the introduction of livestock in the late 1800s. Increases in meadow aridity due to livestock use has been proposed as the primary factor facilitating sagebrush dominance in these areas. However, our data suggest that sagebrush can readily expand into moist meadow areas where the water table is shallow. We explored how the relative importance of local processes influencing seedling establishment vary with changes in site aridity. We quantified patterns of sagebrush abundance in relation to water table depth and surface soil moisture and sagebrush seedling occurrence relative to distance from reproductive sagebrush plants and the presence of gopher disturbance. We tested the independent and interactive effects of vegetation clipping and surface soil disturbances on sagebrush germination, survival, and growth using experiments established in four vegetation types that differed in water table depth, surface soil moisture, and herbaceous species cover. Experiments were con- ducted over two growing seasons that differed in water availability. Our results suggest that small ( , 1m 2 ) soil disturbances promote the germination and growth of sagebrush seedlings in intact, ungrazed, moist, herbaceous meadow areas. In the absence of distur- bance, dense herbs, whether clipped or not, prevented germination. The effects of distur- bance were strongest in sites with moist surface soil that support a dense herbaceous canopy and were less important in sites with lower surface-soil moisture, where seedling estab- lishment rates were low despite abundant exposed soil. The spatial distribution of sagebrush seedlings is consistent with these experimental results. Sagebrush seedling density decreased dramatically with distance from reproductive shrubs, and seedlings were almost always preferentially associated with gopher mounds in moist herbaceous areas. Clipping above- ground biomass of herbs on a relatively small scale (4 m 2 ) had no effect on sagebrush germination or early seedling growth; however, the growth and survival of larger trans- planted seedlings was enhanced by clipping. We conclude that, while sagebrush expansion is traditionally associated with increased meadow aridity, it exhibits the greatest potential for seedling germination, growth, and survival in mesic, rather than xeric, sites. Realization of this potential is dependent on the confluence of exposed soil, a nearby seed source, and reduction of aboveground herb biomass.

Network structure beyond food webs: mapping non-trophic and trophic interactions on Chilean rocky shores

How multiple types of non-trophic interactions map onto trophic networks in real communities remains largely unknown. We present the first effort, to our knowledge, describing a comprehensive ecological network that includes all known trophic and diverse non-trophic links among >100 coexisting species for the marine rocky intertidal community of the central Chilean coast. Our results suggest that non-trophic interactions exhibit highly nonrandom structures both alone and with respect to food web structure. The occurrence of different types of interactions, relative to all possible links, was well predicted by trophic structure and simple traits of the source and target species. In this community, competition for space and positive interactions related to habitat/refuge provisioning by sessile and/or basal species were by far the most abundant non-trophic interactions. If these patterns are orroborated in other ecosystems, they may suggest potentially important dynamic constraints on the combined architecture of trophic and non-trophic interactions. The nonrandom patterning of non-trophic interactions suggests a path forward for developing a more comprehensive ecological network theory to predict the functioning and resilience of ecological communities.

How Structured Is the Entangled Bank? The Surprisingly Simple Organization of Multiplex Ecological Networks Leads to Increased Persistence and Resilience.

Species are linked to each other by a myriad of positive and negative interactions. This complex spectrum of interactions constitutes a network of links that mediates ecological communities’ response to perturbations, such as exploitation and climate change. In the last decades, there have been great advances in the study of intricate ecological networks. We have, nonetheless, lacked both the data and the tools to more rigorously understand the patterning of multiple interaction types between species (i.e., “multiplex networks”), as well as their consequences for community dynamics. Using network statistical modeling applied to a comprehensive ecological network, which includes trophic and diverse non-trophic links, we provide a first glimpse at what the full “entangled bank” of species looks like. The community exhibits clear multidimensional structure, which is taxonomically coherent and broadly predictable from species traits. Moreover, dynamic simulations suggest that this non-random patterning of how diverse non-trophic interactions map onto the food web could allow for higher species persistence and higher total biomass than expected by chance and tends to promote a higher robustness to extinctions.

RESPONSE OF HERBS TO SHRUB REMOVAL ACROSS NATURAL AND EXPERIMENTAL VARIATION IN SOIL MOISTURE

Like many semiarid grasslands, large montane meadows of the Sierra Nevada Mountains, California (USA) have experienced widespread expansion of woody plants (here Rothrock sagebrush, or Artemisia rothrockii), a reduction in herbaceous species cover, and apparent aridification over the past century. Because soil moisture is an important limiting resource in this system, we investigated the interactive effects of shrub removal and soil moisture on herbaceous species recovery. We conducted replicated shrub removal experiments across four sagebrush habitats that differed in soil moisture, water table depth, and related characteristics (e.g., soil texture, initial total herbaceous cover, and initial shrub biomass). Changes in herb cover after shrub removal were monitored over four years that differed in spring snow pack, a critical source of water in this system. To more directly quantify the effects of soil moisture on shrub–herb competition, shrub removal was combined with experimental water addition in the m...