Can we predict nutrient limitation in streams and rivers?

1. Anthropogenic impacts on the biogeochemical cycles of nitrogen (N) and phosphorus (P) affect natural ecosystems worldwide. Modelling is required to predict where and when these key nutrients limit primary production in freshwaters. 2. We reviewed 382 nutrient‐enrichment experiments to examine which factors promote limitation of microphytobenthos biomass by N or P in streams and rivers. Using regression models, we examined whether the response of microphytobenthos biomass to N and P additions could be predicted by the absolute N and P concentrations in the water, the water N:P ratio or a combination of the two. 3. The absolute N concentration in the water was the best predictor of the magnitude of the response of microphytobenthos biomass to N additions. In comparison, the N:P ratio was the best predictor of whether or not N was limiting. However, predictions were uncertain except at extreme N:P ratios <1 : 1 and >100 : 1. 4. The absolute P concentration in the water was the best predictor of the magnitude of the response of microphytobenthos biomass to P additions. Neither the absolute nor the relative N and P concentrations predicted whether or not P was limiting. 5. The absolute and the relative N and P water concentrations contribute significant and complementary insights into the responses of microphytobenthos biomass to nutrient enrichment in running waters. However, ability to predict nutrient limitation from these concentrations is constrained by substantial error in the models. In the future, the prediction ability of models of nutrient limitation might be improved by focussing on regional scales and accounting for additional factors such as light and disturbance.     

Is the relation between nutrient supply and biodiversity co‐determined by the type of nutrient limitation?

Correlative studies have shown a ‘hump‐backed’ relation between the vegetation N:P ratio and plant species diversity with the highest diversity at balanced N:P ratios (between 10 and 14). We tested the hypothesis that adding growth‐limiting nutrients to mesotrophic grasslands that were in shortage of either N (N:P ratio<10) or P (N:P ratio>14) would lead to an increase of plant diversity. Thereto, we studied the effects of long‐term (11 yr) experimentally increased N and/or P supply on soil nutrient pools, vegetation nutrient dynamics and biodiversity in a riverine grassland in the Netherlands with a low soil N:P ratio (N shortage) and a peat grassland with a high soil N:P ratio (P shortage), respectively. Eleven years of nutrient addition hardly had any effects on the total stocks of C, N and P in the soils of both sites, due to the large size of the soil nutrient pools already present and to the management at both sites (annual hay‐making and ‐removal). However, in the riverine grassland the treatments increased the cycling of the small pool of labile N and P compounds resulting in large increases in annual fluxes of especially N. In the unfertilised controls, species establishments balanced more or less species losses during an 11 year period, thus leading to a dynamic equilibrium of the species pool. However, contrary to our hypothesis, addition of the growth‐limiting nutrient led at both sites to a reduction of species diversity even when total biomass remained below critical levels. Species diversity and species evenness were strongly determined by N mineralisation and to a lesser extent by total soil N and extractable P, respectively. Total aboveground biomass of the vegetation was determined by total soil N. Our study shows that patterns found in correlative studies of the relation between plant diversity and soil and vegetation N:P ratio can not be translated into successful experimental manipulations to enhance biodiversity. The most likely explanation is that colonization limitation occurred in the fertilized plots and that not sufficient diaspores of potentially new species could reach and/or colonize the plots to compensate for the species extinctions as a result of increased nutrient supply.     

Does water stress, nutrient limitation, or H-toxicity explain the differential stature among Heath Forest types in Central Kalimantan, Indonesia?

To investigate the causes of the reduced stature of heath forest compared to lowland evergreen rain forest (LERF), the quantity and quality of small litterfall (LF), the standing crop of litter on the forest floor (LSC), and the annual rates of litter decay were determined over a period of 12 months in three contrasting lowland rain forest types in Central Kalimantan, Indonesia. In addition, a litterbag experiment monitored the mass loss of leaves from three dominant tree species in two heath forests (HF) of contrasting stature. Soil water and shallow groundwater dynamics in the two HFs were monitored as well. LF in the LERF was higher compared to both tall heath forest (THF) and relatively stunted heath forest (SHF), but did not differ between the two HFs. Stand-level nutrient-use efficiencies for nitrogen and phosphorus were greatest for the SHF, followed by the THF and the LERF, respectively. The observed differences in nutrient-use efficiency between the two HFs did not result in different LF totals, LSC or decomposition rates and hence cannot explain the difference in HF stature. Neither could phenolic concentrations in leaf LF, which were very similar for the two HFs. Top-soil moisture levels were consistently higher in the SHF compared to the THF and never reached wilting point in either forest type whereas shallow groundwater levels in the SHF were both closer to the surface and more persistent than in the THF. Thus, severe water stress is not thought to be a factor of importance determining HF stature. Rather, considering the much lower pH of the topsoil in the SHF compared to the THF it is hypothesized that different degrees of H-toxicity to fine roots may ultimately prove responsible for the contrast in HF stature.     

Does anthropogenic nitrogen deposition induce phosphorus limitation in herbivorous insects?

Anthropogenic nitrogen deposition has shifted many ecosystems from nitrogen (N) limitation to phosphorus (P) limitation. Although well documented in plants, no study to date has explored whether N deposition exacerbates P limitation at higher trophic levels, or focused on the effects of induced plant P limitation on trophic interactions. Insect herbivores exhibit strict N : P homeostasis, and should therefore be very sensitive to variations in plant N : P stoichiometry and prone to experiencing deposition‐induced P limitation. In the current study, we investigated the effects of N deposition and P availability on a plant‐herbivorous insect system. Using common milkweed (Asclepias syriaca) and two of its specialist herbivores, the monarch caterpillar (Danaus plexippus) and milkweed aphid (Aphis asclepiadis) as our study system, we found that experimental N deposition caused P limitation in milkweed plants, but not in either insect species. However, the mechanisms for the lack of P limitation were different for each insect species. The body tissues of A. asclepiadis always exhibited higher N : P ratios than that of the host plant, suggesting that the N demand of this species exceeds P demand, even under high N deposition levels. For D. plexippus, P addition increased the production of latex, which is an important defense negatively affecting D. plexippus growth rate. As a result, we illustrate that P limitation of herbivores is not an inevitable consequence of anthropogenic N deposition in terrestrial systems. Rather, species‐specific demands for nutrients and the defensive responses of plants combine to determine the responses of herbivores to P availability under N deposition.     

Does nitrogen limitation promote intraguild predation in an aphidophagous ladybird?

Reciprocal intraguild predation occurs between the two aphidophagous ladybird beetles Coccinella septempunctata L. and Harmonia axyridis Pallas (Coleoptera: Coccinellidae). However, its direction is asymmetrical; H. axyridis generally acts as an intraguild predator, and C. septempunctata as an intraguild prey. According to Denno and Fagan's prediction that nitrogen shortages in predators may promote intraguild predation, it was hypothesized that growth of intraguild predator H. axyridis is more limited by nitrogen than that of intraguild prey C. septempunctata, and that H. axyridis growth is enhanced by feeding on C. septempunctata compared to feeding on aphids. To determine nitrogen‐limited growth in H. axyridis, the following two predictions were examined. First, it was predicted that the nitrogen content of H. axyridis would be higher than that of C. septempunctata when both feed on aphids. However, nitrogen content did not differ between the two ladybirds. Second, it was predicted that nitrogen‐use efficiency of H. axyridis would be lower than that of C. septempunctata. However, there was no significant difference between species. These results did not support the hypothesis that growth of H. axyridis is more limited by nitrogen than that of C. septempunctata. In addition, the present study showed that dry mass and nitrogen growth of H. axyridis were not enhanced, but rather decreased, by eating high‐nitrogen C. septempunctata, compared to eating low‐nitrogen aphids. Overall, the present study did not support the hypothesis that nitrogen shortages in predators may promote intraguild predation.     

Does phosphorus limitation promote species-rich plant communities?

It is known that the number of limiting nutrients may affect the species richness of plant communities, but it is unclear whether the type of nutrient limitation is also important. I place the results from a study in Patagonia (elsewhere in this issue) in the context of the number and types of nutrients that are limiting. I present four mechanisms through which N or P limitation may potentially influence species richness. These mechanisms are related to: (i) the number of forms in which P or N are present in soil and the plant traits needed to acquire them, (ii) the mechanisms and traits that control species competition and coexistence under N or P limitation, (iii) the regional species pools of plants capable of growing under N- and P-limited conditions, and (iv) the interaction between the type of nutrient limitation and community productivity. It appears likely that P limitation can favour a higher species richness than N limitation, in at least in a variety of low productive plant communities, but evidence to support this conclusion is so far lacking. The four mechanisms proposed here offer a framework for exploring whether the type of nutrient limitation per se, or an interaction with productivity, is a potential driver for variation in species diversity.     

Does domestication process affect stress response in juvenile Eurasian perch Perca fluviatilis?

The objective was to evaluate the impact of domestication process on the physiological stress response of cultured Eurasian perch confronted to a chronic stress situation. Briefly, F1 and F4 juveniles were submitted to chronic confinement and investigated on days 5, 15 and 30. Capture and 15min-anesthesia were imposed on fish to assess the effect of preceding confinement on acute stress response. On day 30, the fish were finally challenged with Aeromonas hydrophila and sampled after 5 and 10 days for immune parameter measurements. Cortisol and glucose levels were not affected by confinement but increased significantly after acute stressor exposure. Moreover, cortisol rise following capture and anesthesia was higher in F1 confined-fish, suggesting that they have previously been affected by chronic confinement. A higher HSP70 level was also observed on day 30 in F1 confined-juveniles. During bacterial challenge, regardless of confinement level, F4 juveniles displayed higher lysozyme activity and agglutination response than F1 which may indicate a higher immune capacity in domesticated fish. In conclusion, chronic confinement stressor induced few physiological responses but may increase the responsiveness to other aquacultural stressors. Domestication process also seems to improve chronic stress resistance, growth as well as the immune status of the fish.     

Does an ecological advantage produce the asymmetric lineage ratio in a harvester ant population?

In dependent-lineage harvester ant populations, two lineages interbreed but are genetically distinct. The offspring of a male and queen of the same lineage are female reproductives; the offspring of a male and queen of different lineages are workers. Geographic surveys have shown asymmetries in the ratio of the two lineages in many harvester ant populations, which may be maintained by an ecological advantage to one of the lineages. Using census data from a long-term study of a dependent-lineage population of the red harvester ant, Pogonomyrmex barbatus, we identified the lineage of 130 colonies sampled in 1997–1999, ranging in age from 1 to 19 years when collected, and 268 colonies sampled in 2010, ranging in age from 1 to 28 years when collected. The ratio of lineages in the study population is similar across an 11-year interval, 0.59 J2 in 1999 and 0.66 J2 in 2010. The rare lineage, J1, had a slightly but significantly higher number of mates of the opposite lineage than the common lineage, J2, and, using data from previous work on reproductive output, higher male production. Mature colonies of the two lineages did not differ in nest mound size, foraging activity, or the propensity to relocate their nests. There were no strong differences in the relative recruitment or survivorship of the two lineages. Our results show no ecological advantage for either lineage, indicating that differences between the lineages in sex ratio allocation may be sufficient to maintain the current asymmetry of the lineage ratio in this population.     

Does constrained oviposition influence offspring sex ratio in the solitary parasitoid wasp Venturia canescens?

Abstract.  1. In haplodiploid organisms, virgin or sperm-depleted females can reproduce but are constrained to produce only male progeny. According to Godfray's constrained model, when p , the proportion of females constrained to produce only male progeny, is not null in a panmictic population, unconstrained females should bias their sex allocation towards females to compensate for the excess of males. These unconstrained females should be able to adjust the sex ratio in response to local variation of p .
2. In this paper an experimental approach is used to test the hypotheses of this model in the solitary endoparasitoid Venturia canescens under both field and laboratory conditions. Specifically, it is tested whether unconstrained females use their encounters with conspecifics (either male or female) to estimate p and then adjust their sex ratio accordingly.
3. As assumed by Godfray's model, constrained females actively search for host patches in the field and under laboratory conditions produce the same number of offspring during their lifetime as unconstrained females. As predicted by the model, unconstrained females produce a sex ratio biased towards females both in the laboratory and in the field.
4. The results show that this bias is not a response to encounters with conspecifics previous to oviposition. The hypothesis that the bias is due to differential mortality between sexes during ontogeny is also rejected. The proportions of constrained ovipositions estimated in two natural populations explain only a small fraction of the sex ratio bias observed in V. canescens.     

How do chronic nutrient loading and the duration of nutrient pulses affect nutrient uptake in headwater streams?

Our study aimed to analyze the effects of chronic nutrient loading on the capacity of headwater streams to retain phosphorus and ammonium pulses of different duration. For this purpose, we selected nine headwater streams located across a gradient of increasing agricultural land use and eutrophication. In each stream, we performed sequential plateau additions with increasing nutrient concentrations in summer 2015 and instantaneous slug additions in summer 2016 under similar hydrological conditions. We modelled kinetic uptake curves from the slug additions via the Tracer Additions for Spiraling Curve Characterization method and calculated ambient uptake parameters. Ambient uptake rates generally increased (1.4–20.8 µg m^?2 s^?1 for NH₄–N and 0.3–10.3 µg m^?2 s^?1 for SRP, respectively), while ambient uptake velocities decreased from oligotrophic to polytrophic streams (1.8–14.0 mm min^?1 for NH₄–N and 1.6–9.9 mm min^?1 for SRP, respectively). However, correlations between ambient uptake parameters and background concentrations were weak. Concentration-dependent uptake rates followed either a linear or a Michaelis–Menten saturation model, regardless of the degree of nutrient loading. Uptake rate curves showed counter-clockwise hysteresis in oligotrophic streams and clockwise hysteresis in streams of higher trophic states, indicating a reduced significance of hyporheic uptake with increasing nutrient loading. Comparisons of slug and plateau additions revealed that oligotrophic streams were most efficient in uptake during short nutrient pulses, while eutrophic streams profited from longer pulse duration. The results indicate that nutrient uptake is increasingly transport-controlled in polluted streams where increased biofilm thickness and clogging of sediments restrict nutrient transport to reactive sites.     

Can the meiotic sex ratio explain the sex ratio bias in adult populations in the dioicous moss Drepanocladus lycopodioides?

Sex ratio variation is commonly observed in natural populations of many organisms with separate sexes and genetic sex determination, including bryophytes. Most bryophyte populations exhibit female-skewed expressed adult sex ratios, generally inferred from counts of sexually mature plants. For the rarely sexually reproducing perennial dioicous moss Drepanocladus lycopodioides, we showed that a female bias also exists in the genetic adult sex ratio, using a specifically designed molecular sex-associated marker. Here, we investigated whether the meiotic spore sex ratio contributes to the observed bias in genetic adult sex ratio in natural populations. Earlier attempts to study meiotic sex ratios have involved commonly cultivated ruderals that rapidly express sex in the laboratory. We established single-spore cultures from field-collected sporophytes from these populations and used the marker to assess the sex of individual sporelings. Spore germinability was (near) complete, and mortality among sporelings was virtually absent. The true meiotic sex ratio did not differ from equality, but strongly differed both from the observed genetic sex ratios in the natural adult populations, and from the European scale genetic sex ratio. We conclude that the biased population sex ratios in this species arise at life cycle stages after spore germination. Sexual dimorphism may selectively favour female proliferation during some phase of gametophyte development. Based on methodological progress, we successfully used a perennial study species with rare sexual reproduction, which significantly broadens the life history spectrum investigated in bryophyte sex ratio studies.     

Induction of RpoS-dependent functions in glucose-limited continuous culture: what level of nutrient limitation induces the stationary phase of Escherichia coli?

treA and osmY expression and RpoS protein levels were investigated in glucose-limited continuous culture. The level of induction of these stationary-phase markers became as high during growth at a D of 0.1 to 0.2 h(-1) as in carbon-starved batch cultures but only in rpoS+ bacteria. The stress protectant trehalose was actually produced at higher levels at low growth rates than in stationary-phase cultures. The pattern of induction of RpoS-dependent activities could be separated from those regulated by cyclic AMP (cAMP) or endoinduction, and the induction occurred at extreme glucose limitation. Escherichia coli turns to a protective stationary-phase response when nutrient levels fall below approximately 10(-7) M glucose, which is insufficient to saturate scavenger transporters regulated by cAMP plus endoinducers, and this response is optimally expressed at 10(-6) M glucose. The high-level induction of protective functions also explains the maintenance energy requirement of bacterial growth at low dilution rates.     

Nectar to improve parasitoid fitness in biological control: Does the sucrose:hexose ratio matter?

The consumption of saccharide-rich foods such as floral nectar is crucial for the survival of many adult parasitoid wasps. The importance to parasitoids of nectar quality, with regards to its sucrose:hexose ratio, was investigated. Nectar, an aqueous solution of sugars, amino acids and other compounds, differs between plant species. Nectar composition is dominated by sucrose, glucose and fructose. Previous studies have shown that the ratio of sucrose to hexose (glucose+fructose) sugars can explain nectar associations in a range of flower visiting arthropods. It has been suggested that this ratio may be important in terms of parasitoid fitness. Analysis of floral nectar from fourteen plant species confirmed that the sucrose/hexose ratio significantly differed between species. An opportunity to select floral resources based on this measure of nectar quality arose and highlighted the potential to utilize native flowering plant species in place of the seven most commonly deployed, which are usually not native to the countries in which they are used.Results presented in this paper indicate, however, that the sucrose/hexose ratio is not a significant factor explaining parasitoid longevity. The hymenopteran parasitoids Diadegma semiclausum (Ichneumonidae) and Dolichogenidea tasmanica (Braconidae) were fed 40% w/w sugar solutions, differing in their sugar ratios. Solutions were classified as either sucrose-dominant (ratio >0.99), sucrose-rich (ratio 0.5–0.99), hexose-rich (ratio 0.1–0.499) or hexose-dominant (ratio <0.1). No significant differences in parasitoid longevity were found between the different treatments for either species. This suggests there is not an optimal sucrose/hexose ratio for parasitoid wasps, although a greater number of parasitoid species should ideally be tested to confirm if this is true for the wider parasitoid taxonomic groups.     

Does rapid utilization of elevated nutrient availability allow eucalypts to dominate in the tropical savannas of Australia?

Northern Australia's savannas are among the most fire‐prone biomes on Earth and are dominated by eucalypts (Eucalyptus and Corymbia spp.). It is not clear what processes allow this group to dominate under such extreme fire frequencies and whether a superior ability to compete for nutrients and water might play a role. There is evidence that eucalypts are adapted to frequent fires; juvenile eucalypts escape the fire trap by growing rapidly in height between fires. However, non‐eucalypts are less able to escape the fire trap and tend to have stand structures strongly skewed toward suppressed juveniles. The mechanisms that drive these contrasting fire responses are not well understood. Here, we describe the results of a controlled glasshouse seedling experiment that evaluated the relative importance of nutrient and water availability in determining height growth and biomass growth of two eucalypt and one noneucalypt tree species, common in northern Australian savannas. We demonstrate that growth of eucalypt seedlings is particularly responsive to nutrient addition. Eucalypt seedlings are able to rapidly utilize soil nutrients and accumulate biomass at a much greater rate than noneucalypt seedlings. We suggest that a seasonal spike in nutrient availability creates a nutrient‐rich microsite that allows eucalypt seedlings to rapidly gain height and biomass, increasing their likelihood of establishing successfully and reaching a fire‐resistant size. Our results extend our understanding of how eucalypts dominate northern Australian savannas under extremely high fire frequencies.     

Does the nutrient stoichiometry of primary producers affect the secondary consumer Pleurobrachia pileus?

We investigated whether phosphorus limitations of primary producers propagate upwards through the food web, not only to the primary consumer level but also onto the secondary consumers’ level. A tri-trophic food chain was used to assess the effects of phosphorus-limited phytoplankton (the cryptophyte Rhodomonas salina) on herbivorous zooplankters (the copepod Acartia tonsa) and finally on zooplanktivores (the ctenophore Pleurobrachia pileus). The algae were cultured in phosphorus-replete and phosphorus-limited media before being fed to two groups of copepods. The copepods in turn were fed to the top predator, P. pileus, in a mixture resulting in a phosphorus-gradient, ranging from copepods having received only phosphorus-replete algae to copepods reared solely on phosphorus-limited algae. The C:P ratio of the algae varied significantly between the two treatments, resulting in higher C:P ratios for those copepods feeding on phosphorus-limited algae, albeit with a significance of 0.07. The differences in the feeding environment of the copepods could be followed to Pleurobrachia pileus. Contrary to our expectations, we found that phosphorus-limited copepods represented a higher quality food source for P. pileus, as shown by the better condition (expressed as nucleic acid content) of the ctenophore. This could possibly be explained by the rather high C:P ratios of ctenophores, their resulting low phosphorus demand and relative insensitivity to P deficiency. This might potentially be an additional explanation for the observed increasing abundances of gelatinous zooplankton in our increasingly phosphorus-limited coastal seas.