Dynamic responses of phosphorus metabolism to acute and chronic dietary phosphorus-limitation in Daphnia

Food quality is highly dynamic within lake ecosystems and varies spatially and temporally over the growing season. Consumers may need to continuously adjust their metabolism in response to this variation in dietary nutrient content. However, the rates of metabolic responses to changes in food nutrient content has received little direct study. Here, we examine responses in two metabolic phosphorus (P) pools, ribonucleic acids (RNA) and adenosine triphosphate (ATP), along with body mass and body P content in Daphnia magna exposed to chronic and acute dietary P-limitation. First, we examined food quality effects on animals consuming different food carbon (C):P quality over a 14 day period. Then, we raised daphnids on one food quality for 4 days, switched them to contrasting dietary treatments, and measured changes in their metabolic responses at shorter time-scales (over 48 h). Animal P, RNA, and ATP content all changed through ontogeny with adults containing relatively less of these pools with increasing body mass. Irrespective of age, Daphnia consuming high C:P diets had lower body %P, %RNA, %ATP, and mass compared to animals eating low C:P diets. Diet switching experiments revealed diet dependent changes in body %P, %RNA, %ATP, and animal mass within 48 h. We found that Daphnia switched from low to high C:P diets had some metabolic buffering capacity with decreases in body %P occurring after 24 h but mass remaining similar to initial diet conditions for 36 h after the diet switch. Switching Daphnia from low to high C:P diets caused a decrease in the RNA:P ratio after 48 h. Daphnia switched from high to low C:P diets increased their body P, RNA, and ATP content within 8–24 h. This switch from high to low C:P diets also led to increased RNA:P ratios in animal bodies. Overall, our study revealed that consumer P metabolism reflects both current and past diet due to more dynamic and rapid changes in P biochemistry than total body mass. This metabolic flexibility is likely linked to resource integration in D. magna, which reduces the negative effects of short-term or variable exposure to nutrient-deficient foods

Seasonal effects of food quality and temperature on body stoichiometry, biochemistry, and biomass production in Daphnia populations

Food quality and temperature can affect zooplankton production in lakes by altering organismal metabolism. However, the influence of these factors on consumer nutritional physiology and population biomass remains relatively understudied in natural populations. Here, we examined seasonal changes in body stoichiometry, biochemistry, and population biomass in two Daphnia species collected from two separate lakes differing in dietary phosphorus (P) supply. Food quality, measured as seston carbon:P (C:P) ratios, varied throughout the study in each lake, and water temperatures generally increased across the growing season. Daphnid elemental composition was correlated with food quality in both populations, but relationships between daphnid body stoichiometry and temperature were consistently stronger as Daphnia body C:P ratios and content of major biochemical pools declined simultaneously throughout the summer, which largely coincided with increased water temperatures. Warmer temperatures were associated with relaxed %P-RNA coupling as daphnid body RNA content declined and P content remained relatively high. These responses combined with temperature related decreases in Daphnia body %lipids and %C appeared to explain declines in daphnid body C:P ratios in both lakes over the growing season. Seasonal changes in population biomass were related to both food quality and water temperature in the lower nutrient lake. Biomass production under more eutrophic conditions however was unrelated to food quality and was instead associated with seasonal temperature changes in the higher nutrient lake. Overall, our study shows that seasonal changes in temperature and resource quality may differentially affect consumer stoichiometry and biomass production in lake ecosystems by altering consumer elemental metabolism

Interactive effects of genotype and food quality on consumer growth rate and elemental content

Consumer body stoichiometry is a key trait that links organismal physiology to population and ecosystem-level dynamics. However, as elemental composition has traditionally been considered to be constrained within a species, the ecological and evolutionary factors shaping consumer elemental composition have not been clearly resolved. To this end, we examined the causes and extent of variation in the body phosphorus (P) content and the expression of P-linked traits, mass specific growth rate (MSGR), and P use efficiency (PUE) of the keystone aquatic consumer Daphnia using lake surveys and common garden experiments. While daphnid body %P was relatively constrained in field assemblages sampled across an environmental P gradient, unique genotypes isolated from these lakes showed highly variable phenotypic responses when raised across dietary P gradients in the laboratory. Specifically, we observed substantial inter- and intra-specific variation and differences in daphnid responses within and among our study lakes. While variation in Daphnia body %P was mostly due to plastic phenotypic changes, we documented considerable genetic differences in daphnid MSGR and PUE, and relationships between MSGR and body P content were highly variable among genotypes. Overall, our study found that consumer responses to food quality may differ considerably among genotypes and that relationships between organismal life-history traits and body stoichiometry may be strongly influenced by genetic and environmental variation in natural assemblages

Relationships among nutrient enrichment, detritus quality and quantity, and large-bodied shredding insect community structure

Anthropogenic nutrient enrichment of forested headwater streams can enhance detrital quality, decrease standing stocks, and alter the community structure of detrivorous insects, reducing nutrient retention and decreasing ecosystem functioning. Our objective was to determine if stoichiometric principles could be used to predict genus-specific shifts in shredding insect abundance and biomass across a dissolved nutrient and detritus food quality/quantity gradient. Detritus, insect, and water samples were collected from 12 Ozark Highland headwater streams. Significant correlations were found between stream nutrients and detrital quality but not quantity. Abundance and biomass responses of four out of five tested genera were accurately predicted by consumerresource stoichiometric theory. Low carbon:phosphorus (C:P) shredders responded positively to increased total phosphorus and/or food quality, and high C:P shredders exhibited neutral or negative responses to these variables. Genus-specific declines were correlated with decreased overall biomass in shredder assemblages, potentially causing disruptions in nutrient flows to higher level consumers with nutrient enrichment. This work provides further evidence that elevated nutrients may negatively impact shredding insect communities by altering the stoichiometry of detritus–detritivore interactions. A better understanding of stoichiometric mechanisms altering macroinvertebrate populations is needed to help inform water quality criteria for the management of headwater streams

Fear and food: Effects of predator-derived chemical cues and stoichiometric food quality on Daphnia

While resource quality and predator‐derived chemical cues can each have profound effects on zooplankton populations and their function in ecosystems, the strength and direction of their interactive effects remain unclear. We conducted laboratory experiments to evaluate how stoichiometric food quality (i.e., algal carbon [C] : phosphorus [P] ratios) affects responses of the zooplankter, Daphnia pulicaria, to predator‐derived chemical cues. We compared growth rates, body P content, metabolic rates, life‐history shifts, and survival of differentially P‐nourished Daphnia in the presence and absence of chemical cues derived from fish predators. We found effects of predator cues and/or stoichiometric food quality on all measured traits of Daphnia. Exposure to fish cues led to reduced growth and increased metabolic rates but had little effect on the body %P content of Daphnia. Elevated algal C : P ratios reduced growth and body %P and increased mass‐specific respiration rates. While most of the effects of predator cues and algal C : P ratios of Daphnia were non‐interactive, reduced survival and relatedly reduced population growth rates that resulted from P‐poor food were amplified in the presence of predator‐derived cues. Our results demonstrate that stoichiometric food quality interacts with antipredator responses of Daphnia, but these effects are largely trait dependent and appear connected to animal life‐history evolution. Given the ubiquity of predators and P‐poor food in lake ecosystems, our results highlight the importance of the interactive responses of animals to predator cues and poor nutrition

The threshold elemental ratio of carbon and phosphorus of Daphnia magna and its connection to animal growth

The growth of animal consumers is afected by the balance of elements in their diet with the transition between limitation by one element to another known as the threshold elemental ratio (TER). Precise estimates of TERs with known levels of uncertainty have yet to be generated for most zooplankton consumers. We determined the TER for carbon (C) and phosphorus (P) in for a common lake zooplankter, Daphnia magna, using experimental measurements and theoretical considerations. Daphnia growth responses to food C:P ratios across a relatively narrow range (80–350) generated an empirical estimate of TERC:P of 155±14. While this TER matched our modelled estimate of TERC:P (155±16), it was lower than previous estimates of this dietary transition point. No threshold was found when we examined daphnid body C:N or C:P ratios in response to changing food C:P ratios, which indicates P-limitation at even lower food C:P ratios. Our results provide strong evidence that D. magna is likely to experience acute P-limitation when food C:P ratios exceed even relatively low ratios (~155). Our model further demonstrated that while physiological adjustments may reduce the likelihood of P-limitation or reduce its intensity, these changes in animal material processing would be accompanied by reduced maximum growth rates

Mobility and bioavailability of sediment phosphorus in urban stormwater ponds

© 2019. American Geophysical Union. All Rights Reserved. Stormwater ponds can serve as retention hotspots for phosphorus (P) moving out of the urban environment. This retention may be reduced by P speciation that reduces the bioavailability of P to primary producers and alters its mobility in sediments. Here we examined the mobility and fate of dissolved P in urban stormwater ponds with a set of complementary field measurements and short-term laboratory and field experiments. We measured the types and amount of P in water column and sediments of urban stormwater ponds. We further assessed the mobility of different P types in pond sediments in the field and rates of P release from sediment cores maintained under laboratory conditions. Finally, we assessed P uptake rates by pond algal communities using short-term bioassay experiments. We found that dissolved organic P was highly prevalent in urban pond water and sediments and that this type of P was mobile within sediments and could be released under high or low O 2 conditions. We also found highly variable P demand by algae among stormwater ponds and that algal growth responses to P was correlated to water column N:P ratios. Altogether, our results indicate an important role for organic phosphorus cycling in urban stormwater ponds, which likely constrains the overall retention efficiency in these aquatic ecosystems

Leaf-litter stoichiometry is affected by streamwater phosphorus concentrations and litter type

The stoichiometric ratios of organisms and their food resources can influence C and nutrient dynamics in aquatic ecosystems. Several investigators have quantified linkages between nutrient enrichment and consumer stoichiometry for stream detritivores, but very few have systematically quantified the effect of P enrichment on leaf-litter stoichiometry. Here, we examine the potential stoichiometric changes of 2 species of leaf litter subjected to varying levels of P enrichment in laboratory microcosms and mixed species across a natural P gradient of streams in the Ozark Highlands Region, Arkansas, USA. Leaf-litter %P content increased and C:P ratios decreased with increasing levels of P enrichment and with increasing lability of the leaf species. In the laboratory study, C:P of maple and oak leaves in the control treatment was ,2500, whereas this ratio decreased to 500 and 1000 in the high-P treatments, respectively. Total P (TP) was inversely related to leaf-litter C:P along the natural P gradient of streams in the Ozarks. Our results add to the growing body of information on the potential bottom-up effects of anthropogenic nutrient loading in streams and the influence of water-column nutrients and leaf quality on this response

Understanding variation in salamander ionomes: A nutrient balance approach

Ecological stoichiometry uses information on a few key biological elements (C, N, and P) to explain complex ecological patterns. Although factors driving variation in these elements are well-established, expanding stoichiometric principles to explore dynamics of the many other essential elements comprising biological tissues (i.e., the ionome) is needed to determine their metabolic relationships and better understand biological control of elemental flows through ecosystems. 2. In this paper, we report observations of ionomic variation in two species of salamander (Ambystoma opacum and A. talpoideum) across ontogenic stages using specimens from biological collections of two wetlands sampled over a 30-year period. This unique data set allowed us to explore the extent of ionomic variation between species, among ontogenic stages, between sites, and through time. 3. We found species- and to a lesser extent site-specific differences in C, N, and P along with 13 other elements forming salamander ionomes but saw no evidence of temporal changes. Salamander ionomic composition was most strongly related to ontogeny with relatively higher concentrations of many elements in adult males (i.e., Ca, P, S, Mg, Zn, and Cu) compared to metamorphic juveniles, which had greater amounts of C, Fe, and Mn. 4. In addition to patterns of individual elements, covariance among elements was used to construct multi-elemental nutrient balances, which revealed differences in salamander elemental composition between species and sites and changes in elemental proportions across ontogenic development. These multi-elemental balances distinguished among species-site-ontogenic stage groups better than using only C, N, and P. 5. Overall, this study highlights the responsiveness of consumer ionomes to life-history and environmental variation while reflecting underlying relationships among elements tied to biological function. As such, ionomic studies can provide important insights into factors shaping consumer elemental composition and for predicting how these changes might affect higher-order ecological processes

Variation in particulate C : N : P stoichiometry across the Lake Erie watershed from tributaries to its outflow

© 2017 The Authors Limnology and Oceanography published by Wiley Periodicals, Inc. on behalf of Association for the Sciences of Limnology and Oceanography Human activities can cause large alterations in biogeochemical cycles of key nutrients such as carbon (C), nitrogen (N), and phosphorus (P). However, relatively little is known about how these changes alter the proportional fluxes of these elements across ecosystem boundaries from rivers to lakes. Here, we examined environmental factors influencing spatial and temporal variation in particulate C : N : P ratios across the Lake Erie watershed from its tributaries to its outflow. Throughout the study, particulate nutrient ratios ranged widely (C : N 2.0–25.8, C : P 32–530, N : P 3.7–122.9), but mean values were generally lower than previous estimates from different aquatic environments. Particulate C : N ratios varied the least across all environments, but C : P and N : P ratios increased between tributaries and coastal areas and throughout the growing season in coastal environments. These ratios also differed temporally in offshore waters as particulate C : P and N : P were higher in the spring and summer and lower in the fall and winter. Particulate C : P ratios also increased between the western/central and eastern basins indicating differential nutrient processing across the lake. These stoichiometric changes were associated with unique environmental factors among ecosystems as tributary stoichiometry was related to terrestrial land use and land cover, coastal ratios were a product of mixing between riverine and offshore waters, and offshore patterns were influenced by differences in temperature and particulate nutrient loading among basins. Overall, by studying changes in particulate C : N : P ratios across the Lake Erie watershed, our study demonstrates the power of using mass balance principles to study nutrient transformations along the aquatic continuum