Jonathan B. Shurin

Trophic Downgrading of Planet Earth

Until recently, large apex consumers were ubiquitous across the globe and had been for millions of years. The loss of these animals may be humankind’s most pervasive influence on nature. Although such losses are widely viewed as an ethical and aesthetic problem, recent research reveals extensive cascading effects of their disappearance in marine, terrestrial, and freshwater ecosystems worldwide. This empirical work supports long-standing theory about the role of top-down forcing in ecosystems but also highlights the unanticipated impacts of trophic cascades on processes as diverse as the dynamics of disease, wildfire, carbon sequestration, invasive species, and biogeochemical cycles. These findings emphasize the urgent need for interdisciplinary research to forecast the effects of trophic downgrading on process, function, and resilience in global ecosystems.

WHAT DETERMINES THE STRENGTH OF A TROPHIC CASCADE

Trophic cascades have been documented in a diversity of ecological systems and can be important in determining biomass distribution within a community. To date, the literature on trophic cascades has focused on whether and in which systems cascades occur. Many biological (e.g., productivity : biomass ratios) and methodological (e.g., experiment size or duration) factors vary with the ecosystem in which data were collected, but ecosystem type, per se, does not provide mechanistic insights into factors controlling cascade strength. Here, we tested various hypotheses about why trophic cascades occur and what determines their magnitude using data from 114 studies that measured the indirect trophic effects of predators on plant community biomass in seven aquatic and terrestrial ecosystems. Using meta-analysis, we examined the relationship between the indirect effect of predator ma- nipulation on plants and 18 biological and methodological factors quantified from these studies. We found, in contrast to predictions, that high system productivity and low species diversity do not consistently generate larger trophic cascades. A combination of herbivore and predator metabolic factors and predator taxonomy (vertebrate vs. invertebrate) explained 31% of the variation in cascade strength among all 114 studies. Within systems, 18% of the variation in cascade strength was explained with similar predator and herbivore char- acteristics. Within and across all systems, the strongest cascades occurred in association with invertebrate herbivores and endothermic vertebrate predators. These associations may result from a combination of true biological differences among species with different phys- iological requirements and bias among organisms studied in different systems. Thus, al- though cascade strength can be described by biological characteristics of predators and herbivores, future research on indirect trophic effects must further examine biological and methodological differences among studies and systems.

Nutrient co-limitation of primary producer communities.

Synergistic interactions between multiple limiting resources are common, highlighting the importance of co-limitation as a constraint on primary production. Our concept of resource limitation has shifted over the past two decades from an earlier paradigm of single-resource limitation towards concepts of co-limitation by multiple resources, which are predicted by various theories. Herein, we summarise multiple-resource limitation responses in plant communities using a dataset of 641 studies that applied factorial addition of nitrogen (N) and phosphorus (P) in freshwater, marine and terrestrial systems. We found that more than half of the studies displayed some type of synergistic response to N and P addition. We found support for strict definitions of co-limitation in 28% of the studies: i.e. community biomass responded to only combined N and P addition, or to both N and P when added separately. Our results highlight the importance of interactions between N and P in regulating primary producer community biomass and point to the need for future studies that address the multiple mechanisms that could lead to different types of co-limitation.

All wet or dried up? Real differences between aquatic and terrestrial food webs

Ecologists have greatly advanced our understanding of the processes that regulate trophic structure and dynamics in ecosystems. However, the causes of systematic variation among ecosystems remain controversial and poorly elucidated. Contrasts between aquatic and terrestrial ecosystems in particular have inspired much speculation, but only recent empirical quantification. Here, we review evidence for systematic differences in energy flow and biomass partitioning between producers and herbivores, detritus and decomposers, and higher trophic levels. The magnitudes of different trophic pathways vary considerably, with less herbivory, more decomposers and more detrital accumulation on land. Aquatic–terrestrial differences are consistent across the global range of primary productivity, indicating that structural contrasts between the two systems are preserved despite large variation in energy input. We argue that variable selective forces drive differences in plant allocation patterns in aquatic and terrestrial environments that propagate upward to shape food webs. The small size and lack of structural tissues in phytoplankton mean that aquatic primary producers achieve faster growth rates and are more nutritious to heterotrophs than their terrestrial counterparts. Plankton food webs are also strongly size-structured, while size and trophic position are less strongly correlated in most terrestrial (and many benthic) habitats. The available data indicate that contrasts between aquatic and terrestrial food webs are driven primarily by the growth rate, size and nutritional quality of autotrophs. Differences in food-web architecture (food chain length, the prevalence of omnivory, specialization or anti-predator defences) may arise as a consequence of systematic variation in the character of the producer community.

Dispersal limitation, invasion resistance, and the structure of pond zooplankton communities

For a species to colonize a site it must both arrive there by dispersal from another site and maintain positive population growth in the local environment. I experi- mentally tested the role of dispersal limitation in structuring the zooplankton communities of fishless ponds in southwestern Michigan. An average of 12.9 new species of rotifers and crustaceans from the region were introduced at the beginning of the experiment into the intact resident communities of seven ponds in large in situ enclosures (the invasion treatment). Introduced species were found at least once over three months in six of the seven ponds, and one species consistently colonized all three replicate enclosures in three of the ponds. However, the success rate of the introductions was low as >91 % of the species introduced immediately became extinct. In addition, introduced species remained rare throughout the experiment in every pond, comprising only 0-2.5% of total zooplankton community biomass. No effects of the invasion treatment were detected on total zooplankton diversity or biomass, on the biomass of native species, or on chlorophyll a concentration, suggesting that relaxing dispersal limitation for the regional pool had minimal effects on local community structure. Both the biomass of exotic species and the proportion of species introduced that successfully colonized the invasion treatment were negatively correlated with native species diversity. These patterns support the hypothesis that diversity confers resistance to invasion. The results of the invasion treatment indicated a minor role for dispersal limitation in structuring pond zooplankton communities. To test the role of interactions with resident species in excluding potential invaders, a second experiment was performed in four different ponds the following year. In addition to the control and invasion treatment, a second treatment (the resistance treatment) was imposed where the abundance of native species was reduced by filtering before the intro- duction of invaders. The goal of this treatment was to weaken interactions between resident species and invaders while maintaining the abiotic environment intact. Among the four ponds, 3.8 times more exotic species were found in the resistance treatment than in the invasion treatment, and their total biomass was 16.4 times greater. The contrast between the invasion and resistance treatments indicated an important role for species interactions in repelling invaders. The two experiments showed that zooplankton communities were nearly saturated with species and that biotic interactions excluded many potential invaders.

Evolutionary diversification in stickleback affects ecosystem functioning

Explaining the ecological causes of evolutionary diversification is a major focus of biology, but surprisingly little has been said about the effects of evolutionary diversification on ecosystems. The number of species in an ecosystem and their traits are key predictors of many ecosystem-level processes, such as rates of productivity, biomass sequestration and decomposition. Here we demonstrate short-term ecosystem-level effects of adaptive radiation in the threespine stickleback (Gasterosteus aculeatus) over the past 10,000 years. These fish have undergone recent parallel diversification in several lakes in coastal British Columbia, resulting in the formation of two specialized species (benthic and limnetic) from a generalist ancestor. Using a mesocosm experiment, we demonstrate that this diversification has strong effects on ecosystems, affecting prey community structure, total primary production, and the nature of dissolved organic materials that regulate the spectral properties of light transmission in the system. However, these ecosystem effects do not simply increase in their relative strength with increasing specialization and species richness; instead, they reflect the complex and indirect consequences of ecosystem engineering by sticklebacks. It is well known that ecological factors influence adaptive radiation. We demonstrate that adaptive radiation, even over short timescales, can have profound effects on ecosystems.

Consumer versus resource control of producer diversity depends on ecosystem type and producer community structure

Consumer and resource control of diversity in plant communities have long been treated as alternative hypotheses. However, experimental and theoretical evidence suggests that herbivores and nutrient resources interactively regulate the number and relative abundance of coexisting plant species. Experiments have yielded divergent and often contradictory responses within and among ecosystems, and no effort has to date reconciled this empirical variation within a general framework. Using data from 274 experiments from marine, freshwater, and terrestrial ecosystems, we present a cross-system analysis of producer diversity responses to local manipulations of resource supply and/or herbivory. Effects of herbivory and fertilization on producer richness differed substantially between systems: (i) herbivores reduced species richness in freshwater but tended to increase richness in terrestrial systems; (ii) fertilization increased richness in freshwater systems but reduced richness on land. Fertilization consistently reduced evenness, whereas herbivores increased evenness only in marine and terrestrial ecosystems. Producer community evenness and ecosystem productivity mediated fertilization and herbivore effects on diversity across ecosystems. Herbivores increased producer richness in more productive habitats and in producer assemblages with low evenness. These same assemblages also showed the strongest reduction in richness with fertilization, whereas fertilization increased (and herbivory decreased) richness in producer assemblages with high evenness. Our study indicates that system productivity and producer evenness determine the direction and magnitude of top-down and bottom-up control of diversity and may reconcile divergent empirical results within and among ecosystems.

TROPHIC LEVELS AND TROPHIC TANGLES: THE PREVALENCE OF OMNIVORY IN REAL FOOD WEBS

The concept of trophic levels is one of the oldest in ecology and informs our understanding of energy flow and top-down control within food webs, but it has been criticized for ignoring omnivory. We tested whether trophic levels were apparent in 58 real food webs in four habitat types by examining patterns of trophic position. A large proportion of taxa (64.4%) occupied integer trophic positions, suggesting that discrete trophic levels do exist. Importantly however, the majority of those trophic positions were aggregated around integer values of 0 and 1, representing plants and herbivores. For the majority of the real food webs considered here, secondary consumers were no more likely to occupy an integer trophic position than in randomized food webs. This means that, above the herbivore trophic level, food webs are better characterized as a tangled web of omnivores. Omnivory was most common in marine systems, rarest in streams, and intermediate in lakes and terrestrial food webs. Trophic-level-based concepts such as trophic cascades may apply to systems with short food chains, but they become less valid as food chains lengthen.

LOCAL AND REGIONAL ZOOPLANKTON SPECIES RICHNESS: A SCALE-INDEPENDENT TEST FOR SATURATION

Assemblages of coexisting species are formed by immigration from a re- gional pool of colonists and local interactions among species and with the physical envi- ronment. Theory suggests that the shape of the relationship between regional and local species richness may indicate the relative roles of dispersal and local interactions in limiting local diversity. Here we examine patterns of regional and local species richness in freshwater crustacean zooplankton to test whether linear (suggesting dispersal limitation) or curvilinear (suggesting saturation, via strong local control) functions best fit the data. Local richness appeared saturated when regions of different spatial extents were included on the same graph. However, this pattern was influenced by differences in scale among surveys. We corrected for the effects of regional scale by plotting mean local richness against the residuals of the species-landscape area relations. Controlling for the extent of the regional scale produced much more linear patterns, suggesting strong dispersal limitation. We present a simple graphical model to explain how variation among surveys in the geographic size of regions can produce apparent saturation of local diversity even if the underlying pattern of local and regional richness is linear. We also compare the predictive power of residual regional richness on local richness with that of several local features in a multiple regression model. Local richness exhibits strong relationships with both residual regional richness and pH. We argue that the relative strengths of local and regional processes depend on the definition of the regional scale. A variety of evidence suggests that local processes play a major role in generating differences in zooplankton diversity among lakes within a bio- geographic region. Evidence for the importance of dispersal limitation comes largely from comparisons of lakes across very large scales. Our analysis suggests that linear patterns of local and regional diversity are not incompatible with strong local interactions.

Spatial autocorrelation and dispersal limitation in freshwater organisms

Dispersal can limit the ranges of species and the diversity of communities. Despite its importance, little is known about its role in freshwater habitats and its relation to habitat type (lentic vs. lotic), especially for organisms with cryptic dispersal methods such as plankton. Poor dispersers are expected to show more clumped distributions or greater spatial autocorrelation (SA) in community composition than good dispersers. We examined patterns of SA across freshwater taxa with different dispersal modes (active vs. passive) and their association with habitat type (lake vs. stream) using 18 spatially explicit community composition data sets. We found significant relationships between SA and body size among taxa in lake habitats, but not in streams. However, the increase in SA with body size in lakes was driven entirely by fishes—organisms ranging in size from diatoms to macro-invertebrates showed equivalent levels of SA. These results support the idea that large organisms are less effective dispersers in aquatic environments, resulting in greater SA in community structure over broad scales. Streams may be effectively more connected than lakes as patterns of SA and body size were weaker in lotic habitats. Our data suggest that the critical threshold where greater body size increases dispersal limitation seems to come at the juncture between invertebrates and vertebrates rather than that between unicellular and multicellular organisms as has been previously suggested.