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Humans are modifying the availability of nutrients such as nitrogen (N) and phosphorus (P), and it is therefore important to understand how these nutrients, independently or in combination, influence the growth and nutrient content of primary producers. Using meta-analysis of 118 field and laboratory experiments in freshwater, marine and terrestrial ecosystems, we tested hypotheses about co-limitation of N and P by comparing the effects of adding N alone, P alone, and both N and P together on internal N (e.g. %N, C:N) and P (e.g. %P, C:P) concentrations in autotroph communities. In particular, we tested the following predictions. First, if only one nutrient was limiting, addition of that nutrient should decrease the concentration of the other nutrient, but addition of the non-limiting nutrient would have no effect on the internal concentration of the limiting nutrient. If community co-limitation was occurring then addition of either nutrient should result in a decrease in the internal concentration of the other nutrient. Community co-limitation could also result in no change – or even an increase – in N concentrations in response to P addition if P stimulated growth of N fixers. Finally, if biochemically dependent co-limitation was occurring, addition of a limiting nutrient would not decrease, and could even increase, the concentration of the other, co-limited nutrient. We found no general evidence for the decrease in the internal concentration of one nutrient due to addition of another nutrient. The one exception to this overall pattern was marine systems, where N addition decreased internal P concentrations. In contrast, P addition increased internal N concentrations across all experiments, consistent with co-limitation. These results have important implications for understanding the roles that N and P play in controlling producer growth and internal nutrient accumulation as well as for managing the effects of nutrient enrichment in ecosystems. Synthesis On a global scale, humans have doubled nitrogen (N) inputs and quadrupled phosphorus (P) inputs relative to pre-industrial levels. N and P fertilization influences autotroph internal nutrient concentrations and ratios and thereby affects a variety of community and ecosystem processes, including decomposition and consumer population dynamics. It is therefore critical to understand the effects of nutrient additions on the growth and nutrient concentrations of primary producers. We used meta-analysis to evaluate the responses of autotroph internal N and P concentrations to additions of N, P, and N+P and make inferences about limitation and co-limitation of N and P across marine, terrestrial, and freshwater ecosystems. We found little evidence for single-nutrient limitation, highlighting the fact that multiple nutrients generally limit primary production.

Synthesis The tissue chemistry of plants can influence ecosystem processes including growth, herbivory, and decomposition. Our comparison of nitrogen and phosphorus in over 1700 autotroph taxa demonstrates that latitudinal trends in tissue chemistry are consistent across non-vascular and vascular species in freshwater, terrestrial, and marine ecosystems. Tissue chemistry varies most within species and taxonomic lineages, yet the nitrogen to phosphorus ratio within individuals is strikingly similar among species in different ecosystems. These results shed new light on existing hypotheses, suggesting that light (e.g. photon flux) and growing season duration are primary drivers of latitudinal gradients in tissue chemistry, but providing little support for temperature, nutrient supply, or soil substrate age. Photoautotroph nitrogen (N) and phosphorus (P) tissue concentrations can influence ecosystem function via processes including growth, decomposition, and consumption, and may reflect traits maintaining coexistence. Studies in terrestrial systems have led to hypotheses that latitudinal trends in the N and P content of leaves may be driven by soil substrate age, environmental temperature, or season length; however, terrestrial patterns alone cannot differentiate these mechanisms. Here, we demonstrate that broad geographical patterns of N and P in freshwater and marine multicellular photoautotrophs are concordant with those in terrestrial ecosystems. Our > 6800 record database reveals that mean tissue N and P increase with latitude in all ecosystems, but P increases more rapidly, causing N:P to decline; mean N:P scaling within individuals also is identical among systems, despite very different evolutionary environments. A partitioning of the variance in these data suggests that species composition and local environmental context likely lead to the variation observed within a latitudinal band. However, the consistency of trends in photosynthetic tissue chemistry across Earth’s ecosystems suggests that biogeographical gradients in insolation and growing season length may constrain tissue N and P, whereas global trends in temperature, nutrient supply, and soil substrate age are unlikely to generate the consistent latitudinal trends among ecosystems. Thus, this cross-ecosystem comparison suggests a new hypothesis, global patterns of insolation, while also providing a new perspective on other mechanisms that have been hypothesized to underlie latitudinal trends in photosynthetic tissue chemistry.

Ecology Letters (2011) 14: 852–862 Abstract 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.

Summary 1 Foraging by geese has led to vegetation loss in salt marshes along the Hudson Bay coast and lesser snow geese are increasingly grazing inland freshwater marshes. We determined whether different nutrients limit the growth of forage plants in the two habitats, and whether these differences affect the nutritional quality of vegetation available to geese at La Perouse Bay, Manitoba. 2 Results from fertilization experiments indicate that primary productivity in the salt marsh is both nitrogen and phosphorus limited, whereas the freshwater marsh is phosphorus limited. Total amounts of calcium, magnesium and potassium in above-ground biomass per unit area showed similar differences in limitation. 3 Leaves of preferred forage species have higher nutrient concentrations (nitrogen, phosphorus, calcium, potassium, magnesium, sodium) and lower C : N and C : P ratios than alternative forage. The main forage species in the salt marsh ( Puccinellia phryganodes ) has higher nutrient content per unit mass, for nitrogen, magnesium, calcium and sodium, than the major freshwater marsh species( Carex aquatilis ). The difference in nutritional quality of forage between the marshes is likely to have had consequences for goose fitness, and may have contributed to the reported declines in gosling survivorship and size. 4 At moderate grazing intensities, seasonal growth of salt-marsh forage is maintained by addition of nitrogen and, to a lesser extent, phosphorus from high numbers of goose faeces to swards. In contrast, the low densities and low phosphorus content of goose faeces in the phosphorus-limited freshwater marsh mean that plants are unlikely to recover rapidly from the effects of grazing. As a consequence, the freshwater marsh is likely to become increasingly less productive as foraging intensifies. 5 Nutrient gradients in vegetation across an ecotone and changes in foraging behaviour have resulted in adverse effects on both the growth rates of individuals and the population structure of a herbivore.

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.