Paul C. Frost

ROSEMARY MACKAY FUND ARTICLE: Ecological stoichiometry of trophic interactions in the benthos: understanding the role of C:N:P ratios in lentic and lotic habitats

This paper considers how the theory of ecological stoichiometry may be applied to issues of importance to benthic ecologists. Ecological stoichiometry considers both the causes of elemental (C:N:P) imbalances between trophic levels and their consequences on foodweb dynamics (e.g., predator–prey interactions) and ecosystem processes (e.g., nutrient cycling). Elemental imbalances are created between consumers and their food, in part, by the accumulation of C relative to other nutrients (N and P) in benthic organic matter as a result of the deposition of detritus and/or unbalanced growth in aquatic producers. High C:N and C:P ratios in food material can reduce growth and reproduction and alter related processes such as nutrient release in benthic consumers. By affecting consumer metabolism, elemental imbalances may affect population dynamics, trophic interactions, and gross transfer efficiencies in benthic systems. Future work is needed to quantify the frequency and magnitude of elemental imbalances, to determine why elemental ratios differ within and among trophic levels, and to examine how stoichiometric imbalances affect fundamental ecosystem processes (e.g., nutrient cycling and spiraling, consumer growth dynamics, and responses to environmental disturbance) in benthic systems.

JOINT EFFECTS OF UV RADIATION AND PHOSPHORUS SUPPLY ON ALGAL GROWTH RATE AND ELEMENTAL COMPOSITION

Abstratct. Phytoplankton growth and elemental composition are influenced by a number of factors such as photosynthetically active radiation (PAR) and nutrient availability. However, little is known about the influence of solar ultraviolet radiation (UVR) and interactions with nutrients on algal growth processes in situ. We tested the effects of solar radiation and phosphorus supply on algal growth kinetics and elemental composition in two boreal lakes (northwestern Ontario, Canada) during summer 1999. Growth bioassays (at five phosphorus concentrations) assessed changes in algal growth and elemental composition exposed to (1) ultraviolet A [UVA], ultraviolet B [UVB], and photosynthetically active radiation [PAR], (2) UVA and PAR, and (3) PAR only. Growth rates, calculated from changes in seston carbon and chlorophyll, responded strongly to both P and UVR. Results indicated that phytoplankton growth was co-regulated by P limitation and UVR suppression, with highest growth rates found in high P, low UVR treatments. Phytoplankton exposed to both UVA and UVB generally grew more slowly than those exposed to PAR only, even at high P levels. UVB and UVA reduced maximum growth rates by 8-66% and 1 1-21 %, respectively. Phytoplankton growth was more strongly affected by UVB in spring than later in summer, possibly due to shifts in the dominant species present. Manipulations of light and P supply both significantly affected seston C:P ratios. UVR reduced sestonic C:P. Such changes in growth rates and C:P ratios from UVR exposure may have important implications for pelagic food web dynamics.

RESPONSES OF A BACTERIAL PATHOGEN TO PHOSPHORUS LIMITATION OF ITS AQUATIC INVERTEBRATE HOST

Host nutrition is thought to affect the establishment, persistence, and severity of pathogenic infections. Nutrient-deficient foods possibly benefit pathogens by constraining host immune function or benefit hosts by limiting parasite growth and reproduction. However, the effects of poor elemental food quality on a hosts susceptibility to infection and disease have received little study. Here we show that the bacterial microparasite Pasteuria ramosa is affected by the elemental nutrition of its aquatic invertebrate host, Daphnia magna. We found that high food carbon:phosphorus (C:P) ratios significantly reduced infection rates of Pasteuria in Daphnia and led to lower within-host pathogen multiplication. In addition, greater virulent effects of bacterial infection on host reproduction were found in Daphnia-consuming P-deficient food. Poor Daphnia elemental nutrition thus reduced the growth and reproduction of its bacterial parasite, Pasteuria. The effects of poor host nutrition on the pathogen were further evidenced by Pasteurias greater inhibition of reproduction in P-limited Daphnia. Our results provide strong evidence that elemental food quality can significantly influence the incidence and intensity of infectious disease in invertebrate hosts.

Elemental Composition of Littoral Invertebrates from Oligotrophic and Eutrophic Canadian Lakes

The P, N, and C content of littoral macroinvertebrates from 8 lakes located in 3 distinct geographical regions of Canada (central Alberta, northwestern Ontario, and Rocky Mountains near Jasper, Alberta) is described. A wide range of values was found in the body content (all values are % of dry mass) of P (0.4-1.6%), N (5.8-13.7%), and C (32.5-53.5%) in the data set containing invertebrates from all 8 lakes. C:P (63-324), N:P (9.6-60), and C:N (4.2-7.6) (all by atom) also varied widely. This variation was partly related to the different mean body content of P, N, and C among taxonomic groups. However, the mean P, N, and C content of macroinvertebrate assemblages varied little among lakes. The patterns of elemental composition in benthic invertebrates shown here are similar to zoo-plankton and terrestrial insects, and indicate that the strength of stoichiometric constraints acting in littoral food webs will depend on the taxa being considered.

UV RADIATION, PHOSPHORUS, AND THEIR COMBINED EFFECTS ON THE TAXONOMIC COMPOSITION OF PHYTOPLANKTON IN A BOREAL LAKE1

We examined how UV radiation and phosphorus (P) affect the taxonomic composition, abundance, and biomass of phytoplankton in an oligotrophic boreal lake. We exposed phytoplankton to three different solar radiation regimes (PAR + UV‐A radiation [UVAR]+ UV‐B radiation [UVBR], PAR + UVAR, and PAR only) and to five levels of P. The biomass of small chrysophytes was reduced by 350% after exposure to PAR + UVAR + UVBR compared with PAR only. No other taxa were found to be negatively affected by exposure to UVBR. Several taxa (e.g. Chry‐ sochromulina laurentiana Kling) were sensitive to UVAR, whereas others (e.g. Tabellaria flocculosa (Roth) Kutzing) were not affected by UV radiation exposure. Principal components analysis ordination separated phytoplankton that were negatively affected by UV radiation and/or positively affected by P treatments (e.g. small chrysophytes, Cryptomonas rostratiformis, T. flocculosa) from those that generally were unaffected by either treatment (e.g. desmids, some Cyanobacteria). Richness, Shannon‐Weaver diversity, and evenness were significantly higher in phytoplankton communities shielded from UVAR and UVBR. The relationship between diversity and richness was positive in all phytoplankton samples except in those exposed to UVBR. Thus, UVBR‐exposed phytoplankton communities were dominated by a few species even though the number of taxa remained relatively unchanged. Consequently, alterations in the UV environments of lakes resulting from climate warming (e.g. drought) and land‐use change (e.g. increased P export) will likely promote shifts in the community composition of lake phytoplankton.

Transgenerational effects of poor elemental food quality on Daphnia magna

Environmental effects on parents can strongly affect the phenotype of their offspring, which alters the heritability of traits and the offspring’s responses to the environment. We examined whether P limitation of the aquatic invertebrate, Daphnia magna, alters the responses of its offspring to inadequate P nutrition. Mother Daphnia consuming P-poor algal food produced smaller neonates having lower body P content compared to control (P-rich) mothers. These offspring from P-stressed mothers, when fed P-rich food, grew faster and reproduced on the same schedule as those from P-sufficient mothers. In contrast, offspring from P-stressed mothers, when fed P-poor food, grew more slowly and had delayed reproduction compared to their sisters born to control mothers. There was also weak evidence that daughters from P-stressed mothers are more susceptible to infection by the virulent bacterium, Pasteuria ramosa. Our results show that P stress is not only transferred across generations, but also that its effect on the offspring generation varies depending upon the quality of their own environment. Maternal P nutrition can thus determine the nature of offspring responses to food P content and potentially obfuscates relationships between the performance of offspring and their own nutrition. Given that food quality can be highly variable within and among natural environments, our results demonstrate that maternal effects should be included as an additional dimension into studies of how elemental nutrition affects the physiology, ecology, and evolution of animal consumers.

Ecological stoichiometry of indirect grazer effects on periphyton nutrient content

Ecological stoichiometry has been successful in enhancing our understanding of trophic interactions between consumer and prey species. Consumer and prey dynamics have been shown to depend on the nutrient composition of the prey relative to the nutrient demand of the consumer. Since most experiments on this topic used a single consumer species, little is known about the validity of stoichiometric constraints on trophic interactions across consumers and ecosystems. We conducted a quantitative meta-analysis on grazer–periphyton experiments to test (1) if benthic grazers have consistent effects on the nutrient composition of their prey, and (2) whether these effects can be aligned to the nutrient stoichiometry of grazer and periphyton, other environmental factors, or experimental constraints. Grazers significantly lowered periphyton C:N and C:P ratios, indicating higher N- and P-content of grazed periphyton across studies. Grazer presence on average increased periphyton N:P ratios, but across studies the effect size did not differ significantly from zero. The sign and strength of grazer effects on periphyton nutrient ratios was strongly dependent on the nutrient content of grazers and their food, but also on grazer biomass, the amount of biomass removal and water column nutrients. Grazer with low P-content tended to reduce periphyton P-content, whereas grazers with high P-content increased periphyton P-content. This result suggests that low grazer P-content can be an indication of physiological P-limitation rather than a result of having relatively low and fixed P-requirements. At the across-system scale of this meta-analysis, predictions from stoichiometric theory are corroborated, but the plasticity of the consumer nutrient composition has to be acknowledged.

Nutritional indicators and their uses in ecology

The nutrition of animal consumers is an important regulator of ecological processes due to its effects on their physiology, life-history and behaviour. Understanding the ecological effects of poor nutrition depends on correctly diagnosing the nature and strength of nutritional limitation. Despite the need to assess nutritional limitation, current approaches to delineating nutritional constraints can be non-specific and imprecise. Here, we consider the need and potential to develop new complementary approaches to the study of nutritional constraints on animal consumers by studying and using a suite of established and emerging biochemical and molecular responses. These nutritional indicators include gene expression, transcript regulators, protein profiling and activity, and gross biochemical and elemental composition. The potential applications of nutritional indicators to ecological studies are highlighted to demonstrate the value that this approach would have to future studies in community and ecosystem ecology.

The interaction between cyanobacteria and zooplankton in a more eutrophic world

As blooms of cyanobacteria expand and intensify in freshwater systems globally, there is increasing interest in their ecological effects. In addition to being public health hazards, cyanobacteria have long been considered a poor quality food for key zooplankton grazers that link phytoplankton to higher trophic levels. While past laboratory studies have found negative effects of nutritional constraints and defensive traits (i.e., toxicity and colonial or filamentous morphology) on the fitness of large generalist grazers (i.e., Daphnia), cyanobacterial blooms often co-exist with high biomass of small-bodied zooplankton in nature. Indeed, recent studies highlight the remarkable diversity and flexibility in zooplankton responses to cyanobacterial prey. Reviewed here are results from a wide range of laboratory and field experiments examining the interaction of cyanobacteria and a diverse zooplankton taxa including cladocerans, copepods, and heterotrophic protists from temperate to tropical freshwater systems. This synthesis shows that longer exposure to cyanobacteria can shift zooplankton communities toward better-adapted species, select for more tolerant genotypes within a species, and induce traits within the lifetime of individual zooplankton. In turn, the function of bloom-dominated plankton ecosystems, the coupling between primary producers and grazers, the stability of blooms, and the potential to use top down biomanipulation for controlling cyanobacteria depend largely on the species, abundance, and traits of interacting cyanobacteria and zooplankton. Understanding the drivers and consequences of zooplankton traits, such as physiological detoxification and selective vs. generalist grazing behavior, are therefore of major importance for future studies. Ultimately, co-evolutionary dynamics between cyanobacteria and their grazers may emerge as a critical regulator of blooms.

Watershed discharge modulates relationships between landscape components and nutrient ratios in stream seston

In order to understand the environmental controls of the elemental composition of suspended particles in streams and rivers, we examined relationships between the stoichiometry of suspended particles and catchment characteristics (e.g., topography and land cover) under contrasting hydrological conditions in streams from the Upper Peninsula of Michigan, USA. Particulate C:N, N:P, and C:P ratios varied considerably among streams on each of 10 separate sampling dates and within most streams through time. When averaged across the study period by stream, particulate C:N:P ratios were strongly related to several catchment properties. For example, particulate C:P and N:P ratios were negatively related to the percentage of catchment used for agriculture but positively related to the percentage of catchment found as wetlands. These relationships reflected, in part, variable concentrations of mineral particles, which were strongly related to stream length, agriculture, and upstream lake area. In addition, the strength of the relationships between particulate elemental composition and catchment properties changed depending upon hydrologic condition of the Ontonagon watershed. For example, periods of wetness, as indicated by high river discharge, were found to increase the strength of seston C:N ratio-percentage of wetlands relationships but to reduce the strength of seston C:P ratios-percentage of wetlands relationships. Our results thus demonstrate that the balance of elements fluxing through forested streams is strongly affected by catchment properties but that these effects are sensitive to watershed discharge. At times of high discharge, there are strong connections to catchment sources while in-stream processes appear to predominate at time of low discharge.