Consumer-driven Nutrient Recycling Research Articles

Consumer-driven nutrient recycling of freshwater decapods: Linking ecological theories and application in integrated multitrophic aquaculture.

The Metabolic Theory of Ecology (MTE) and the Ecological Stoichiometry Theory (EST) are central and complementary in the consumer-driven recycling conceptual basis. The understanding of physiological processes of organisms is essential to explore and predict nutrient recycling behavior, and to design integrated productive systems that efficiently use the nutrient inputs through an adjusted mass balance. We fed with fish-feed three species of decapods (prawn, anomuran, crab) from different families and with aquacultural potential to explore the animal-mediated nutrient dynamic and its applicability in productive systems. We tested whether body mass, body elemental content, and feeds predict N and P excretion rates and ratios within taxa. We also verified if body content scales allometrically with body mass within taxa. Finally, we compared the nutrient excretion rates and body elemental content among taxa. N excretion rates of prawns and anomurans were negatively related to body mass, emphasizing the importance of MTE. Feed interacted with body mass to explain P excretion of anomurans and N excretion of crabs. Body C:N content positively scaled with body mass in prawns and crabs. Among taxa, prawns mineralised more N and N:P, and less P, and exhibited higher N and C body content (and lower C:N) than the other decapods. Body P and N:P content were different among all species. Body content and body mass were the main factors that explained the differences among taxa and influence the role of crustaceans as nutrient recyclers. These features should be considered to select complementary species that efficiently use feed resources. Prawns need more protein in feed and might be integrated with fish of higher N-requirements, in contrast to crabs and anomurans. Our study contributed to the background of MTE and EST through empirical data obtained from decapods and it provided insightful information to achieve more efficient aquaculture integration systems.

Ecological Stoichiometery and Consumer-Driven Nutrient Recycling by Elliptio complanata (Lightfoot) in a Northeastern Coastal Zone Pond

Freshwater mussels recycle nutrients within their environment, and the extent of their influence depends on ambient nutrient concentrations and time of year. This study investigated the stoichiometry of consumer-driven nutrient recycling (C, N, and P) of the numerically dominant indigenous freshwater mussel Elliptio complanata (Eastern Elliptio) in a New England pond, which we accomplished by evaluating the stoichiometry of seston, mussel tissues, excretion, and biodeposition. Based on our results, we identified 4 major findings. First, we found seston CNP was not variable across seasons as expected, with only 4 of 10 pairwise interactions being statistically significant, and did not necessarily match the Redfield ratio as expected with higher C:N and lower C:P and N:P observations. Second, we found our tissue CNP to be below the expected 106:16:1 Redfield ratio and that the mussels did not adhere to strict stoichiometric homeostasis throughout different sizes/ages, as shown with 5 of 12 regressions being statistically significant. Third, we found freshwater mussel excretion to be similar to that found in other studies and that excretion rates and ratios were influenced by size and shifted with changes in season—possibly related to seston composition as well as environmental conditions such as temperature, based on 7 of 10 statistical analyzes being significant. Finally, we found freshwater mussel biodeposition to be variable across time for nutrient rates and ratios as we expected.

Phytoplankton growth and stoichiometric responses to warming, nutrient addition and grazing depend on lake productivity and cell size.

Global change involves shifts in multiple environmental factors that act in concert to shape ecological systems in ways that depend on local biotic and abiotic conditions. Little is known about the effects of combined global change stressors on phytoplankton communities, and particularly how these are mediated by distinct community properties such as productivity, grazing pressure and size distribution. Here, we tested for the effects of warming and eutrophication on phytoplankton net growth rate and C:N:P stoichiometry in two phytoplankton cell size fractions (<30 µm and >30 µm) in the presence and absence of grazing in microcosm experiments. Because effects may also depend on lake productivity, we used phytoplankton communities from three Dutch lakes spanning a trophic gradient. We measured the response of each community to multifactorial combinations of temperature, nutrient, and grazing treatments and found that nutrients elevated net growth rates and reduced carbon:nutrient ratios of all three phytoplankton communities. Warming effects on growth and stoichiometry depended on nutrient supply and lake productivity, with enhanced growth in the most productive community dominated by cyanobacteria, and strongest stoichiometric responses in the most oligotrophic community at ambient nutrient levels. Grazing effects were also most evident in the most oligotrophic community, with reduced net growth rates and phytoplankton C:P stoichiometry that suggests consumer‐driven nutrient recycling. Our experiments indicate that stoichiometric responses to warming and interactions with nutrient addition and grazing are not universal but depend on lake productivity and cell size distribution.

Consumption explains intraspecific variation in nutrient recycling stoichiometry in a desert fish.

Consumer-driven nutrient recycling can have substantial effects on primary production and patterns of nutrient limitation in aquatic ecosystems by altering the rates as well as the relative supplies of the key nutrients nitrogen (N) and phosphorus (P). While variation in nutrient recycling stoichiometry has been well-studied among species, the mechanisms that explain intraspecific variation in recycling N:P are not well-understood. We examined the relative importance of potential drivers of variation in nutrient recycling by the fish Gambusia marshi among aquatic habitats in the Cuatro Ciénegas basin of Coahuila, Mexico. There, G.marshi inhabits warm thermal springs with high predation pressure as well as cooler, surface runoff-fed systems with low predation pressure. We hypothesized that variation in food consumption among these habitats would drive intraspecific differences in excretion rates and N:P ratios. Stoichiometric models predicted that temperature alone should not cause substantial variation in excretion N:P, but that further reducing consumption rates should substantially increase excretion N:P. We performed temperature and diet ration manipulation experiments in the laboratory and found strong support for model predictions. We then tested these predictions in the field by measuring nutrient recycling rates and ratios as well as body stoichiometry of fish from nine sites that vary in temperature and predation pressure. Fish from warm, high-predation sites excreted nutrients at a lower N:P ratio than fish from cool, low-predation sites, consistent with the hypothesis that reduced consumption under reduced predation pressure had stronger consequences for P retention and excretion among populations than did variation in body stoichiometry. These results highlight the utility of stoichiometric models for predicting variation in consumer-driven nutrient recycling within a phenotypically variable species.

Exploited and excreting: parasite type affects host nutrient recycling.

Parasite-induced changes in the nutrient balance of hosts could alter the availability of nutrients in ecosystems by changing consumer-driven nutrient recycling. While these effects on host nutrient use are mediated by host physiology, they likely depend on characteristics of the parasite and host diet quality. We examined this possibility by measuring nutrient release rates of uninfected Daphnia and conspecifics infected by two microparasites (the bacterium Pasteuria ramosa and the microsporidium Hamiltosporidium tvaerminnensis) from daphnid hosts fed food that varied in phosphorus content. We found that infection type and diet affected host nutrient release rates, but the strength of these effects varied among parasite treatments. To improve our understanding of these effects, we examined whether two separate aspects of host exploitation (parasite-induced reductions in host fecundity and parasite load) could account for variation in Daphnia nutrient release, ingestion, and elemental ratios caused by our infection and diet treatments. Regardless of whether we compared individuals across infection type or diet treatment, Daphnia fecundity described variation in multiple aspects of host nutrient use better than infection, diet, or spore load. Our results suggest that parasite-induced changes in host nutrient use are both parasite and diet specific, and that host fecundity could be a useful parameter for predicting the magnitude and direction of these changes.

Woodstoich III: Integrating tools of nutritional geometry and ecological stoichiometry to advance nutrient budgeting and the prediction of consumer‐driven nutrient recycling

Within the last two decades, ecological stoichiometry (ES) and nutritional geometry (NG, also known as geometric framework for nutrition) have delivered novel insights into core questions of nutritional ecology. These two nutritionally explicit frameworks differ in the ‘nutrient currency’ used and the focus of their past research; behavioural feeding strategies in NG, mainly investigating terrestrial organisms, and trophic ecology in ES, mainly in aquatic settings. However, both NG and ES have developed in explaining patterns across various scales of biological organization. Integrating specific tools of these frameworks could advance the field of nutritional ecology by unifying theoretical and empirical approaches from the organismal to ecosystem level processes. Toward this integration, we identified 1) nutrient/element budgets as a shared concept of both frameworks that encompass nutrient intake, retention, and release, 2) response surface plots of NG as powerful tools to illustrate processes at the organismal level and 3) the concept of consumer‐driven nutrient recycling (CNR) of ES as a useful tool bridging organism and ecosystem scales. We applied response surface plots to element budget data from an ES study to show how this approach can deliver new insights at the organismal level, e.g. by showing the interplay between egestion and excretion depending simultaneously on the consumed amount of carbon and phosphorus based on variation across individuals. By integrating concepts of ES and NG to model microbial uptake and mineralization of nitrogenous wastes reported in a NG study, we also demonstrate that considering biochemically explicit mineralization rates of organic wastes can improve predictions of CNR by reducing over‐ or underestimation of mineralization depending on the quality of the consumer's diet. Our presented tools and approaches can help to bridge the organismal and ecosystem level, advancing the predictive power of studies in nutritional ecology at multiple ecological scales.

Differences in phosphorus use between ancient and extant Daphnia genotypes alters algal stoichiometry and abundance

Understanding the ecological relevance of intraspecific variation and evolutionary change in traits is a central frontier in contemporary ecology. Ecological stoichiometry uses variation in the content and kinetics of elements among species to predict key ecological functions such as nutrient recycling. Although much work has focused on interspecific variation, little is known about the ecological consequences of intraspecific variation and evolutionary change in the processing of ecologically relevant elements such as phosphorus (P). We tested whether physiological evolution can alter somatic P content of Daphnia and algal stoichiometry and abundance as predicted by stoichiometric models of consumer-driven nutrient recycling. We used genotypes of Daphnia pulicaria hatched from resting eggs in lake sediments separated by several hundreds of years of evolution in the wild. Although no significant differences were observed in somatic P content of genotypes from different sediment layers, radiotracer (33P) assays in 2 P–supply conditions (HiP and LoP) revealed considerable differences in P incorporation, particularly under HiP conditions. Further, algae co-occurring with the modern, P-inefficient Daphnia genotypes contained more 33P and exhibited faster population growth compared to counterparts co-occurring with ancient, P-efficient genotypes, with differences more prominent under HiP conditions. This study highlights the potential for intraspecific variation in P-use physiology in affecting trophic interactions via consumer-driven nutrient recycling. Melding ecological stoichiometry and resurrection ecology should elucidate the evolutionary sources and ecological consequences of such variation.

Genotypic differences in phosphorus use physiology in producers (Chlamydomonas reinhardtii) and consumers (Daphnia pulex) interact to alter primary and secondary production

By considering the relative abundance of elements in trophic interactions, ecological stoichiometry makes predictions about key ecological processes such as biomass production and consumer-driven nutrient recycling. Theoretical and empirical work has focused on interspecific variation in elemental composition, and stoichiometric imbalances between resources and consumers in determining productivity, particularly at the base of foodwebs. Recent work has found considerable intraspecific variation in elemental composition. We know little about the ecological relevance of such variation, and whether predictions of stoichiometric theory hold at the intraspecific level. Here, we used two genotypes of a primary producer Chlamydomonasreinhardtii, and two genotypes of a primary consumer Daphnia pulex, which are already known to vary considerably in their phosphorus (P) use physiology, under conditions of P abundance and limitation, to explore whether such intraspecific differences alter primary as well as secondary production. Specifically, we tested whether there are intraspecific differences in the carbon: phosphorus (C:P) stoichiometry of Chlamydomonas genotypes, whether such differences affect growth and abundance of the two Daphnia genotypes, and whether the two Daphnia genotypes had distinct effects on primary production and growth of the two Chlamydomonas genotypes. We found significant differences in C:P stoichiometry between the two Chlamydomonas genotypes in both P supply conditions. Such intraspecific differences altered the growth of Daphnia genotypes, and affected the outcome of genotypic competition. Finally, Daphnia genotype affected primary production, and interacted with P supply to distinctly affect the growth of the two Chlamydomonas genotypes. Together, our results highlight the potential ecological relevance of intraspecific differences in nutrient use physiology and elemental composition, and the utility of ecological stoichiometry in understanding such consequences.

Metabolic stoichiometry and the ecology of fear in Trinidadian guppies: consequences for life histories and stream ecosystems

Consumer-driven nutrient recycling, the release of chemicals as byproducts and excesses of consumer physiology, can alter ecosystems by changing the availability of limiting nutrients at the base of the food web. The mere presence of predators can alter consumer physiology by restricting food intake and inducing stress. Predation risk, then, can influence ecosystem function by modifying the role of prey as nutrient recyclers, yet there are few empirical tests of how predation risk alters nutrient recycling by prey. Here, we present the results of a test for the effects of predation risk on the C and N budgets of Trinidadian guppies (Poecilia reticulata). We reared female guppies for 7 weeks on diets of varying quality, and we compared control individuals to those exposed continuously to chemical cues emitted by a guppy predator, Crenicichla alta. We measured food consumption, growth rate, tissue elemental stoichiometry and N excretion by guppies on all treatments. Guppies strongly reduced food intake in the presence of predator cues; however, cue-exposed guppies assimilated nutrients more efficiently than controls. Specifically, cue-exposed guppies strongly increased N retention efficiency while only moderately increasing C efficiency. Consequently, guppies reared with predator cues excreted 39% less N than control guppies. We suggest that reduced foraging, enhanced nutrient efficiency, and decreased N excretion are adaptive responses to the extrinsic mortality threat posed by guppy predators. The resulting substantial reduction in N excretion by guppies may influence ecosystem function in natural streams by reducing the supply of a limiting nutrient.

Influence of consumer-driven nutrient recycling on primary production and the distribution of N and P in the ocean

Abstract. In this study we investigated the impact of consumer-driven nutrient recycling (CNR) on oceanic primary production and the distribution of nitrogen (N) and phosphorus (P) in the deep ocean. For this purpose, we used and extended two existing models: a 2-box model of N and P cycling in the global ocean (Tyrrell, 1999), and the model of Sterner (1990) which formalised the principles of CNR theory. The resulting model showed that marine herbivores may affect the supply and the stoichiometry of N and P in the ocean, thereby exerting a control on global primary production. The predicted global primary production was higher when herbivores were included in the model, particularly when these herbivores had higher N:P ratios than phytoplankton. This higher primary production was triggered by a low N:P resupply ratio, which, in turn, favoured the P-limited N2-fixation and eventually the N-limited non-fixers. Conversely, phytoplankton with higher N:P ratios increased herbivore yield until phosphorus became the limiting nutrient, thereby favouring herbivores with a low P-requirement. Finally, producer-consumer interactions fed back on the N and P inventories in the deep ocean through differential nutrient recycling. In this model, N deficit or N excess in the deep ocean resulted not only from the balance between N2-fixation and denitrification, but also from CNR, especially when the elemental composition of producers and consumers differed substantially. Although the model is fairly simple, these results emphasize our need for a better understanding of how consumers influence nutrient recycling in the ocean.

Food-web structure and functioning of temperate and tropical lakes: A stoichiometric viewpoint

Difficulties to simply transfer trophic cascade theory from temperate to tropical lakes are now well recognized. Many mechanisms trying to explain top-down divergences between these systems have been proposed, such as lack of key species of herbivorous zooplankton, absence of seasonality in fish reproduction, cyanobacteria development, or differences in fish foraging behaviour. Very few studies have considered bottom-up mechanisms, in particular differences in nutrient recycling and nutrient limitation between the two types of ecosystems. According to the ecological stoichiometry theory, fish-induced alterations of food-web structure could modify the efficiency of consumer-driven nutrient recycling by changing the relative biomass contribution of species in food webs. Consequently, by mostly considering top-down processes, one could underestimate consequences on nutrient availability for phytoplankton growth. In this paper, we compared the results of two mesocosm experiments carried out in temperate and tropical areas, each manipulating food- web structure via the presence or absence of fish. We found trophic cascades in both experiments, but differ- ences between fishless and fish treatments were greater in temperate than in tropical systems. In the tropical experiment, the observed effects could not be supported by classical zooplankton community alteration or by cyanobacteria prevalence. Our results suggest a key contribution of fish nitrogen-excretion to phytoplankton growth in mostly nitrogen-limited tropical systems. Differences in stoichiometric response to food-web structure alteration between temperate and tropical lakes could thus represent a major difference between the two systems. Our study stresses the need for further studies that would allow robust generalization on the functioning of freshwater temperate and tropical ecosystems.

Nutrient release and ecological stoichiometry of freshwater mussels (Mollusca:Unionidae) in 2 small, regionally distinct streams

AbstractEcological stoichiometry is the study of the balance of multiple elements in ecological interactions and processes. We investigated the ecological stoichiometry of freshwater mussels across 3 seasons at 2 sites each in an agricultural watershed (Little Darby Creek [LD], Ohio) and a forested watershed (Upper Ouachita River [OR], Arkansas) (2 species/stream). We used nutrient-release experiments to determine C, N, and P content and elemental ratios in seston and in consumer-driven nutrient recycling (CNR) components (mussel soft tissues, shells, biodeposited material, and excreted nutrients). We focused on seasonal patterns of: 1) biodeposition and excretion rates; 2) seston and CNR component % C, % N, % P, C:N, C:P, and N:P; and 3) degree of homeostasis in mussels. Differences in mass-specific biodeposition and excretion rates were driven largely by seasonal factors. Percent P, C:N, C:P, and N:P of seston were seasonally variable in LD, and % C, % N, % P, C:N, C:P, and N:P of seston were seasonally...

Effects of temporal and spatial heterogeneities created by consumer-driven nutrient recycling on algal diversity

A spatially explicit plant–herbivore model composed of planktonic herbivores, algal preys and nutrients was constructed to examine the effects of consumer-driven nutrient recycling (CNR) on the algal species richness with and without spatial structure. The model assumed that either of two essential nutrients (N and P) limited growth of algal populations and that consumer individuals moved randomly in the lattice and grazed all the algal species with the same efficiency. The results showed that when there was no CNR, the number of persistent algal species was affected by neither supply rates of external nutrients nor spatial structure and was consistently low. When consumers recycled nutrients according to their stoichiometry, the algal species richness changed with supply rates of external nutrients depending on spatial structure: the algal species richness decreased with increasing nutrient loadings when there were no spatial structure because CNR increased the probability of stochastic extinction of algal species by amplifying the oscillation of algae-consumer dynamics. However, when spatial structures were created by the migration of consumers, CNR increased the algal species richness in a range of nutrient loadings because spatial variation of grazing pressure functioned to stabilize the algal-consumer dynamics. The present study suggests that through grazing and nutrient recycling, consumer individuals can create ephemeral heterogeneity in growth environments for algal species and that this ephemerality is one of the keys to understanding algal species in nature.

Stoichiometry of consumer‐driven nutrient recycling across nutrient regimes in streams

Stoichiometric constraints within ecological interactions and their ecosystem consequences may depend on characteristics of the abiotic environment such as background nutrient levels. We assessed whether consumer identity, via differing body stoichiometry, could regulate periphyton stoichiometry across nutrient regimes in open systems. In 60 flow-through artificial streams, we factorially crossed dissolved inorganic nitrogen levels (elevated = 294 micog L(-1), ambient = 26 microg L(-1)) with dissolved inorganic phosphorus levels (DIP: elevated = 15 microg L(-1), ambient = 3 microg L(-1)) and consumer type [crayfish (body N : P = 18), snails (body N : P = 28) or a control]. At ambient DIP, periphyton in the crayfish treatment had a lower %P and a lower C : P than periphyton in the snail treatment suggesting that consumer identity, probably mediated by differing P-excretion, regulated periphyton P content. At high DIP, consumer identity no longer affected periphyton elemental composition. Therefore, the stoichiometry of consumer-driven nutrient recycling and consumer identity may be less important to ecosystem functioning in environments with elevated nutrient levels.

LINKING LIFE HISTORY STRATEGIES AND ONTOGENY IN CRUSTACEAN ZOOPLANKTON: IMPLICATIONS FOR HOMEOSTASIS

Work to date has established that consumers are constrained in their chemical content variability. Such a constraint generates many different kinds of ecological relationships ranging from aspects of animal mineral nutrition to factors affecting consumer-driven nutrient recycling. Although previous studies have shown variation in zooplankton nutrient content within and between taxa, most stoichiometric studies assume that consumers are homeostatic in their elemental composition. In this paper, this assumption is reexamined as we describe the variability in the elemental content of the calanoid copepod Mixodiaptomus laciniatus Lilljeborg throughout its ontogeny (interstage variability) and for its specific developmental stages (intrastage variability). Mean copepod carbon content as dry mass increased significantly during ontogeny from 36.3% in nauplii to 51.5% in immature copepodites and 55.8% in adults. Mean phosphorus content decreased from 0.98% in nauplii to 0.87% in immature copepodites and 0.51% in ...

THE STOICHIOMETRY OF CONSUMER-DRIVEN NUTRIENT RECYCLING: THEORY, OBSERVATIONS, AND CONSEQUENCES

Ecologists are increasingly recognizing the importance of consumers in regulating ecosystem processes such as nutrient cycling. Ecologists have recently made considerable progress in understanding nutrient cycling and trophic interactions in pelagic systems by application of a new concept, ecological stoichiometry, to consumer-driven processes. In this paper we synthesize these conceptual advances within pelagic ecology and attempt to illustrate how they may be usefully applied in other ecosystems. Stoichiometric theory shows that both grazer and algal elemental composition are critical parameters influencing rates and ratios of nutrient release. Thus, the stoichiometry of nutrient recycling is a feedback mechanism linking grazer dynamics and algal nutritional status. Incorporation of such effects into a fully dynamic stoichiometric model generates profound changes in the predicted dynamics of algae and grazers, suggesting that adoption of a stoichiometric view may substantively alter our view of the interaction between trophic dynamics and nutrient cycling. The basic predictions of stoichiometric models of nutrient release are generally supported by experimental data showing that N:P release ratios are primarily a function of algal N:P ratio and secondarily a function of grazer N:P ratio, and that rates of P release by grazers are also related to food P:C. Furthermore, evidence for effects of nutrient release stoichiometry on phytoplankton communities and pelagic ecosystem function is accumulating, including data showing consistent alterations in algal physiological status and ecosystem-scale changes in N fixation in response to altered grazer community structure and elemental composition. As the general features of the stoichiometry of algae–zooplankton interactions reflect fundamental biological processes linked to plant and animal mineral nutrition, the stoichiometric view of consumer-driven nutrient recycling can easily be applied to other ecosystems, including terrestrial and benthic food webs. A suite of potential applications of stoichiometric thinking to benthic and terrestrial habitats is suggested.

The Stoichiometry of Consumer-Driven Nutrient Recycling: Theory, Observations, and Consequences

The Stoichiometry of Consumer-Driven Nutrient Recycling: Theory, Observations, and Consequences