Low investment in sexual reproduction threatens plants adapted to phosphorus limitation

Fujita, Yuki; Venterink, Harry Olde; Bodegom, Peter M. van; Douma, Jacob C.; Heil, G. W.; Hölzel, Norbert; Jabłońska, Ewa; Kotowski, Wiktor; Okruszko, Tomasz; Pawlikowski, Paweł; Ruiter, Peter C. de; Wassen, Martin J.

doi:10.1038/nature12733

Cited by 170 publications

(238 citation statements)

References 41 publications

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“…In two studies, however, a larger number of endangered plant species were found under P‐ than under N‐limited conditions, which suggests that elevated P is more likely to be the cause of species loss than N enrichment (Fujita et al., 2014; Wassen, Venterink, Lapshina, & Tanneberger, 2005). …”

Section: Discussionmentioning

confidence: 99%

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Nitrogen:phosphorous supply ratio and allometry in five alpine plant species

Luo

Mazer

Guo

et al. 2016

Ecology and Evolution

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In terrestrial ecosystems, atmospheric nitrogen (N) deposition has greatly increased N availability relative to other elements, particularly phosphorus (P). Alterations in the availability of N relative to P can affect plant growth rate and functional traits, as well as resource allocation to above‐ versus belowground biomass (M A and M B). Biomass allocation among individual plants is broadly size‐dependent, and this can often be described as an allometric relationship between M A and M B, as represented by the equation MnormalA=αMBnormalβ, or log M A = logα + βlog M B. Here, we investigated whether the scaling exponent or regression slope may be affected by the N:P supply ratio. We hypothesized that the regression slope between M A and M B should be steeper under a high N:P supply ratio due to P limitation, and shallower under a low N:P supply ratio due to N limitation. To test these hypotheses, we experimentally altered the levels of N, P, and the N:P supply ratio (from 1.7:1 to 135:1) provided to five alpine species representing two functional groups (grasses and composite forbs) under greenhouse conditions; we then measured the effects of these treatments on plant morphology and tissue content (SLA, leaf area, and leaf and root N/P concentrations) and on the scaling relationship between M A and M B. Unbalanced N:P supply ratios generally negatively affected plant biomass, leaf area, and tissue nutrient concentration in both grasses and composite forbs. High N:P ratios increased tissue N:P ratios in both functional groups, but more in the two composite forbs than in the grasses. The positive regression slopes between log M A and log M B exhibited by plants raised under a N:P supply ratio of 135:1 were significantly steeper than those observed under the N:P ratio of 1.7:1 and 15:1. Synthesis: Plant biomass allocation is highly plastic in response to variation in the N:P supply ratio. Studies of resource allocation of individual plants should focus on the effects of nutrient ratios as well as the availability of individual elements. The two forb species were more sensitive than grasses to unbalanced N:P supplies. To evaluate the adaptive significance of this plasticity, the effects of unbalanced N:P supply ratio on individual lifetime fitness must be measured.

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Section: Discussionmentioning

confidence: 99%

“…Forbs would therefore be expected to become endangered or at greater risk of extinction than grasses when N:P supply ratios are unbalanced. Consistent with this, endangered species are often small and occur more frequently in environments characterized by high N:P ratios (Fujita et al., 2014). …”

Section: Discussionmentioning

confidence: 99%

Nitrogen:phosphorous supply ratio and allometry in five alpine plant species

Luo

Mazer

Guo

et al. 2016

Ecology and Evolution

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“…For example, if a consumer feeding on N-limited plants (low plant N:P) releases waste products with an even lower N:P than that in plant tissue (following rule 1), the herbivore could render the plant community even more N-limited, which can then impact competitive interactions between plants and plant community composition (Sterner, 1990;Fujita et al, 2014). However, the impact on plant communities will depend on the proportion of nutrient demand met by consumer-driven recycling.…”

Section: Rule 2 (Ecosystem Level)-impact Of N:p Release By Herbivoresmentioning

confidence: 99%

“…However, compared to aquatic systems, the role of terrestrial herbivores in mediating N:P ratios has received little attention so far. Because the ratio of N:P availability influences the type of growth limitation and the functional composition of terrestrial plant communities (Elser et al, 2007;Fujita et al, 2014), we hypothesize that the impact of terrestrial herbivores on this ratio has potentially strong ecosystem consequences.…”

Section: Introductionmentioning

confidence: 99%

The Stoichiometry of Nutrient Release by Terrestrial Herbivores and Its Ecosystem Consequences

et al. 2017

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It is widely recognized that the release of nutrients by herbivores via their waste products strongly impacts nutrient availability for autotrophs. The ratios of nitrogen (N) and phosphorus (P) recycled through herbivore release (i.e., waste N:P) are mainly determined by the stoichiometric composition of the herbivore's food (food N:P) and its body nutrient content (body N:P). Waste N:P can in turn impact autotroph nutrient limitation and productivity. Herbivore-driven nutrient recycling based on stoichiometric principles is dominated by theoretical and experimental research in freshwater systems, in particular interactions between algae and invertebrate herbivores. In terrestrial ecosystems, the impact of herbivores on nutrient cycling and availability is often limited to studying carbon (C):N and C:P ratios, while the role of terrestrial herbivores in mediating N:P ratios is also likely to influence herbivore-driven nutrient recycling. In this review, we use rules and predictions on the stoichiometry of nutrient release originating from algal-based aquatic systems to identify the factors that determine the stoichiometry of nutrient release by herbivores. We then explore how these rules can be used to understand the stoichiometry of nutrient release by terrestrial herbivores, ranging from invertebrates to mammals, and its impact on plant nutrient limitation and productivity. Future studies should focus on measuring both N and P when investigating herbivore-driven nutrient recycling in terrestrial ecosystems, while also taking the form of waste product (urine or feces) and other pathways by which herbivores change nutrients into account, to be able to quantify the impact of waste stoichiometry on plant communities.

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“…This may lead to higher species richness under P-limited than under otherwise comparable N-limited conditions. Fujita et al (2014) found that Plimited conditions favour species that invest little in sexual reproduction and are thus vulnerable to local extinction. Olde Venterink et al (2003) found indications that under P-limited conditions endangered plant species persist at higher production levels than under N-limited conditions.…”

Section: Introductionmentioning

confidence: 99%

Species-rich grassland can persist under nitrogen-rich but phosphorus-limited conditions

et al. 2016

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Aim Deposition of nitrogen is assumed to cause loss of botanical diversity, probably through increased production and exclusion of less competitive species. However, if production is (co-)limited by phosphorus, acceleration of the phosphorus cycle may be responsible for the diversity loss and, where that is the case, nitrogen emission reduction may turn out to be an ineffective mitigation strategy. Here we study the feasibility of this mechanism through adding potassium and phosphorus to grassland where nitrogen limitation is absent. Methods We made vegetation relevés in a long-term agricultural fertilisation experiment where potassium, phosphorus and nitrogen were being added to grassland on drained peat where nitrogen availability was high, even in unfertilised plots. We applied a multivariate analysis to investigate the effect of additions of K, K + P and K + P + N on the species composition. Results Unfertilised plots had a very low biomass production and were rich in plant species despite their high nitrogen availability. Addition of potassium led to a strongly increased production but did not result in a reduction of species numbers. Phosphorus in addition to potassium increased production still further and decreased species numbers, most notably the number of endangered species. Conclusions Even under nitrogen rich conditions species richness may be high in grasslands where phosphorous provides a limitation to plant growth. Phosphorus limitation and phosphorus enrichment are both common in grassland, at least in north-western Europe. Part of the general decrease in species numbers that is commonly ascribed to nitrogen enrichment may therefore be due to phosphorus enrichment. If phosphorus and nitrogen are co-limiting (which is often the case) the current nitrogen emission reduction policies may be effective, but not sufficient to restore grassland diversity to its preindustrial level.

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Low investment in sexual reproduction threatens plants adapted to phosphorus limitation

Cited by 170 publications

References 41 publications

Nitrogen:phosphorous supply ratio and allometry in five alpine plant species

Nitrogen:phosphorous supply ratio and allometry in five alpine plant species

The Stoichiometry of Nutrient Release by Terrestrial Herbivores and Its Ecosystem Consequences

Species-rich grassland can persist under nitrogen-rich but phosphorus-limited conditions

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