Matthew E. S. Bracken

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.

A cross-system synthesis of consumer and nutrient resource control on producer biomass

Nutrient availability and herbivory control the biomass of primary producer communities to varying degrees across ecosystems. Ecological theory, individual experiments in many different systems, and system-specific quantitative reviews have suggested that (i) bottom-up control is pervasive but top-down control is more influential in aquatic habitats relative to terrestrial systems and (ii) bottom-up and top-down forces are interdependent, with statistical interactions that synergize or dampen relative influences on producer biomass. We used simple dynamic models to review ecological mechanisms that generate independent vs. interactive responses of community-level biomass. We calibrated these mechanistic predictions with the metrics of factorial meta-analysis and tested their prevalence across freshwater, marine and terrestrial ecosystems with a comprehensive meta-analysis of 191 factorial manipulations of herbivores and nutrients. Our analysis showed that producer community biomass increased with fertilization across all systems, although increases were greatest in freshwater habitats. Herbivore removal generally increased producer biomass in both freshwater and marine systems, but effects were inconsistent on land. With the exception of marine temperate rocky reef systems that showed positive synergism of nutrient enrichment and herbivore removal, experimental studies showed limited support for statistical interactions between nutrient and herbivory treatments on producer biomass. Top-down control of herbivores, compensatory behaviour of multiple herbivore guilds, spatial and temporal heterogeneity of interactions, and herbivore-mediated nutrient recycling may lower the probability of consistent interactive effects on producer biomass. Continuing studies should expand the temporal and spatial scales of experiments, particularly in understudied terrestrial systems; broaden factorial designs to manipulate independently multiple producer resources (e.g. nitrogen, phosphorus, light), multiple herbivore taxa or guilds (e.g. vertebrates and invertebrates) and multiple trophic levels; and - in addition to measuring producer biomass - assess the responses of species diversity, community composition and nutrient status.

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.

Coastal oceanography sets the pace of rocky intertidal community dynamics

The structure of ecological communities reflects a tension among forces that alter populations. Marine ecologists previously emphasized control by locally operating forces (predation, competition, and disturbance), but newer studies suggest that inputs from large-scale oceanographically modulated subsidies (nutrients, particulates, and propagules) can strongly influence community structure and dynamics. On New Zealand rocky shores, the magnitude of such subsidies differs profoundly between contrasting oceanographic regimes. Community structure, and particularly the pace of community dynamics, differ dramatically between intermittent upwelling regimes compared with relatively persistent down-welling regimes. We suggest that subsidy rates are a key determinant of the intensity of species interactions, and thus of structure in marine systems, and perhaps also nonmarine communities.

Herbivore metabolism and stoichiometry each constrain herbivory at different organizational scales across ecosystems

Plant-herbivore interactions mediate the trophic structure of ecosystems. We use a comprehensive data set extracted from the literature to test the relative explanatory power of two contrasting bodies of ecological theory, the metabolic theory of ecology (MTE) and ecological stoichiometry (ES), for per-capita and population-level rates of herbivory across ecosystems. We found that ambient temperature and herbivore body size (MTE) as well as stoichiometric mismatch (ES) both constrained herbivory, but at different scales of biological organization. Herbivore body size, which varied over 11 orders of magnitude, was the primary factor explaining variation in per-capita rates of herbivory. Stoichiometric mismatch explained more variation in population-level herbivory rates and also in per-capita rates when we examined data from within functionally similar trophic groups (e.g. zooplankton). Thus, predictions from metabolic and stoichiometric theories offer complementary explanations for patterns of herbivory that operate at different scales of biological organization.

Seaweed diversity enhances nitrogen uptake via complementary use of nitrate and ammonium.

The consequences of declining biodiversity remain controversial, in part because many studies focus on a single metric of ecosystem functioning and fail to consider diversitys integrated effects on multiple ecosystem functions. We used tide pool microcosms as a model system to show that different conclusions about the potential effects of producer diversity on ecosystem functioning may result when ecosystem functions are measured separately vs. together. Specifically, we found that in diverse seaweed assemblages, uptake of either nitrate or ammonium alone was equal to the average of the component monocultures. However, when nitrate and ammonium were available simultaneously, uptake by diverse assemblages was 22% greater than the monoculture average because different species were complementary in their use of different nitrogen forms. Our results suggest that when individual species have dominant effects on particular ecosystem processes (i.e., the sampling effect), multivariate complementarity can arise if different species dominate different processes. Further, these results suggest that similar mechanisms (complementary nutrient uptake) may underlie diversity-functioning relationships in both algal and vascular-plant-based systems.

DIVERSITY ENHANCES COVER AND STABILITY OF SEAWEED ASSEMBLAGES: THE ROLE OF HETEROGENEITY AND TIME

Generalizations regarding the mechanisms underlying the effects of plant diversity on ecosystem processes, and whether the patterns transcend study systems remain elusive. Many terrestrial plant diversity manipulations have found that plant biomass increases with diversity, but most marine studies find little or no effect of seaweed diversity on producer biomass or production. However, differences in experimental approach (field vs. mesocosm) and duration (years vs. weeks) between published terrestrial and marine experiments confound the interpretation of these differences in response to changing diversity. We conducted a three-year field manipulation of seaweed diversity on intertidal rocky reefs in central California, USA, to examine the effect of diversity on seaweed cover. We found that diversity increased standing algal cover and decreased the availability of free space relative to monocultures, but this effect took nine months to materialize. Furthermore, diverse assemblages did not consistently exceed the best performing monocultures until 18 months after the experiment was initiated, suggesting that the effect of diversity strengthens over time. Overall, diversitys effect was consistently stronger than that of individual species and not attributable to the influence of any particular species (sampling effect) because (1) polycultures eventually achieved higher cover than even the best performing monoculture and (2) monocultures rarely differed much, precluding a strong sampling effect. Instead, mechanisms such as facilitation and differential use of microhabitats in a heterogeneous environment likely caused the higher cover in polycultures. Our findings contrast with short-term experiments with other seaweeds but are similar to longer-term experiments with terrestrial plants, suggesting that experimental design and approach, rather than inherent differences between marine and terrestrial ecosystems, underlie contrasting responses among systems. We argue that experiments conducted in the field, and for a greater length of time, allow for the manifestation of a greater number of potential mechanisms of overyielding in diverse communities, increasing the likelihood of observing a strong diversity effect.

Complementarity in marine biodiversity manipulations: Reconciling divergent evidence from field and mesocosm experiments

Mounting concern over the loss of marine biodiversity has increased the urgency of understanding its consequences. This urgency spurred the publication of many short-term studies, which often report weak effects of diversity (species richness) driven by the presence of key species (the sampling effect). Longer-term field experiments are slowly accumulating, and they more often report strong diversity effects driven by species complementarity, calling into question the generality of earlier findings. However, differences among study systems in which short- and long-term studies are conducted currently limit our ability to assess whether these differences are simply due to biological or environmental differences among systems. In this paper, we compared the effect of intertidal seaweed species richness on biomass accumulation in mesocosms and field experiments using the same pool of species. We found that seaweed species richness increased biomass accumulation in field experiments in both short (2-month) and long (3-year) experiments, although effects were stronger in the long-term experiment. In contrast, richness had no effect in mesocosm experiments, where biomass accumulation was completely a function of species identity. We argue that the short-term experiments, like many published experiments on the topic, detect only a subset of possible mechanisms that operate in the field over the longer term because they lack sufficient environmental heterogeneity to allow expression of niche differences, and they are of insufficient length to capture population-level responses, such as recruitment. Many published experiments, therefore, likely underestimate the strength of diversity on ecosystem processes in natural ecosystems.

DIVERSITY OF INTERTIDAL MACROALGAE INCREASES WITH NITROGEN LOADING BY INVERTEBRATES

Many ecological phenomena are characterized by context dependency, and the relationship between diversity and productivity is no exception. We examined the re- lationship between macroalgal diversity and nutrient availability by evaluating the effects of reduced nutrients and their subsequent replacement via local-scale nutrient loading in tide pools. Macroalgae in Oregon coast high-intertidal pools have evolved in a nitrate-rich upwelling ecosystem, but instead of settling on low-intertidal reefs (where algae are often immersed in nutrient-rich nearshore waters) these individuals have colonized high-zone pools, where they are isolated from the ocean for extended periods of time and are subjected to extended periods of nitrate depletion. In some pools, this nutrient stress was ameliorated by a positive interaction: the excretion of ammonium by invertebrates. We conducted ex- perimental manipulations to quantify invertebrate-mediated ammonium loading and ma- croalgal ammonium uptake in high-intertidal pools. Variation in tide pool volume and invertebrate biomass created a gradient of local-scale nutrient inputs, allowing us to address the relationship between nitrogen loading and algal diversity. Slow-growing species tolerant of low nitrogen availability were joined by fast-growing species with higher nitrogen re- quirements in pools with higher ammonium loading rates. A fourfold increase in the am- monium loading rate was associated with a doubling in the number of macroalgal species, and macroalgal assemblages in more species-rich pools were characterized by higher rates of biomass-specific ammonium uptake. These patterns contrast with productivity-diversity relationships in terrestrial systems, where local-scale nutrient enrichments generally result in reduced producer diversity due to displacement of subordinate species by aggressive competitors. Our data suggest that the effect of enrichment on diversity is context-depen- dent. Each ecosystem has a critical level of nutrient availability, determined by the level of nutrients typically available in that system. Below this critical level, local-scale nutrient additions increase diversity, but above it, diversity declines with enrichment.

Invertebrate-mediated nutrient loading increases growth of an intertidal macroalga

Even in nitrogen‐replete ecosystems, microhabitats exist where local‐scale nutrient limitation occurs. For example, coastal waters of the northeastern Pacific Ocean are characterized by high nitrate concentrations associated with upwelling. However, macroalgae living in high‐zone tide pools on adjacent rocky shores are isolated from this upwelled nitrate for extended periods of time, leading to nutrient limitation. When high‐intertidal pools are isolated during low tide, invertebrate‐excreted ammonium accumulates, providing a potential nitrogen source for macroalgae. I quantified the influence of mussels (Mytilus californianus Conrad) on ammonium accumulation rates in tide pools. I then evaluated the effects of ammonium loading by mussels on nitrogen assimilation and growth rates of Odonthalia floccosa (Esp.) Falkenb., a common red algal inhabitant of pools on northeastern Pacific rocky shores. Odonthalia was grown in artificial tide pool mesocosms in the presence and absence of mussels. Mesocosms were subjected to a simulated tidal cycle mimicking emersion and immersion patterns of high‐intertidal pools on the central Oregon coast. In the presence of mussels, ammonium accumulated more quickly in the mesocosms, resulting in increased rates of nitrogen assimilation into algal tissues. These increased nitrogen assimilation rates were primarily associated with higher growth rates. In mesocosms containing mussels, Odonthalia individuals added 41% more biomass than in mesocosms without mussels. This direct positive effect of mussels on macroalgal biomass represents an often overlooked interaction between macroalgae and invertebrates. In nutrient‐limited microhabitats, such as high‐intertidal pools, invertebrate‐excreted ammonium is likely an important local‐scale contributor to macroalgal productivity.