Grantee Research Project Results
2006 Progress Report: Linking Food Web Structure, Grazer Toxin Resistance and Ecological Stoichiometry in Understanding Harmful Algal Blooms
EPA Grant Number: R831706Title: Linking Food Web Structure, Grazer Toxin Resistance and Ecological Stoichiometry in Understanding Harmful Algal Blooms
Investigators: Dam, Hans G. , McManus, George , Kremer, Patricia
Institution: University of Connecticut
EPA Project Officer: Packard, Benjamin H
Project Period: January 1, 2005 through December 31, 2007 (Extended to December 31, 2008)
Project Period Covered by this Report: January 1, 2006 through December 31,2007
Project Amount: $408,315
RFA: Ecology and Oceanography of Harmful Algal Blooms (2004) RFA Text | Recipients Lists
Research Category: Aquatic Ecosystems , Water , Environmental Statistics
Objective:
Trophic cascades are evident when removal or addition of a trophic group affects changes at lower trophic levels. We hypothesize that the complex dynamics and feedbacks in trophic cascades determine the formation and fate of harmful algal blooms (HABs), and the trophic transfer of toxins. The main goal of this project is to examine the effects of three feedback factors seldom considered in tandem in the expression of planktonic trophic cascades involving toxic algae: (1) The toxicity of the algae, (2) toxin resistance of grazer populations, and (3) the elemental stoichiometric (C: N: P) imbalance between algae and grazers. We are testing the hypotheses that: (1) Trophic cascades are stronger in the presence of toxic algae. (2) Trophic cascades are weaker in the presence of toxin-resistant grazer populations. (3) The strength of trophic cascades depends on the interaction of the stoichiometric imbalance of the grazers, the toxicity of the algae and the complexity of the foodweb. Tests involve combinations of controlled laboratory, in situ, and microcosm experiments.Progress Summary:
Results to date:
Discovery of copepod toxin resistant phenotypes. This set of experiments was motivated by our desire to use toxin resistant individuals in trophic cascade experiments. We documented for the first time toxin-resistant reproductive phenotypes of copepods, and a novel procedure to identify these phenotypes (Avery and Dam, 2007). Individual copepods of the species Acartia hudsonica were raised on two diets: a standard non-toxic diet and a diet containing the toxic dinoflagellate Alexandrium fundyense, both offered at non-limiting concentrations. Resistant individuals were defined as those that survived on the toxic diet. We examined several life-history characteristics, including survivorship, age at metamorphosis, age at maturity, fecundity, and fitness. During this study, we discovered five resistance-related reproductive phenotypes that appeared as discrete classes in a frequency distribution of fecundity. After grouping the data according to these phenotypes, we calculated the fitness of each phenotype on each diet. We also calculated the cost and advantage associated with resistance. On the standard diet, one phenotype suffered 46% lower fitness than the phenotype with the highest fitness, indicating that possessing resistance alleles can carry a substantial cost. A different phenotype showed maximum relative fitness on the toxic diet and reduced relative fitness on the standard diet. From these results, we argue that resistance is conferred by a simple genetic system showing heterozygote advantage. A polymorphism for resistance will prevent the fixation of resistance alleles in natural populations. It may also confound the interpretation of typical experiments that measure average population responses (Avery and Dam, 2007).
Positive effects of toxin on grazers. We discovered a novel response that will help us to understand the role of grazing in the fate of toxic blooms. In laboratory experiments copepods responded to toxic Alexandrium sp. by increasing survivorship and egg production (Fig. 1). Neither food quality nor food quantity could account for the responses. We propose a physiological mechanism by which ingested toxins improve assimilation efficiency by increasing the residence time of food in the copepod gut. Such positive effects, which are currently unappreciated, will affect grazing feedbacks and therefore, the fate of HABs. Potential positive effects, which are novel responses to paralytic shellfish poisoning toxins, should be considered when evaluating the co-evolution of toxic prey and their consumers.
Fig. 1. Survivorship (left) and egg production and fecal pellet production (right) in the copepod Acartia hudsonica exposed to toxic Alexandrium and a nontoxic diet. From Avery and Dam (submitted).
Toxicity of Alexandrium to ciliates. Experiments were carried out with the ciliate Strombidinopsis sp. fed two members of the Alexandrium fundyense complex, A. fundyense and A. tamarense. A. tamarense is considered to be non-toxic or less toxic than A. fundyense because it does not produce saxitoxin (STX). While both dinoflagellates make other STX-related compounds, A. tamarense produces less of these than A. fundyense. The ciliate fed on both species of Alexandrium. It survived, but did not grow on A. fundyense; however, there was significant mortality in ciliates fed A. tamarense (Fig. 2). Behavioral assays showed unexpected differences in reactions of ciliates to A. fundyense and A. tamarense extracts, with avoidance (backwards swimming) induced by fresh A. tamarense extract but not A. fundyense, and backwards swimming induced by both extracts when aged. We are presently developing further the behavior assay and evaluating the effects of calcium channel blockers on motility and grazing in planktonic ciliates to assess the role of this interaction in promoting harmful algal blooms.
Fig. 2. Growth rate versus food type in 45 h assays. Rhodo= Rhodomonas, a nontoxic food.
Effects of omnivory and stoichiometric imbalance on copepod feeding: One aspect of food web complexity, omnivory, is predicted to dampen trophic cascades, whereas stoichiometric imbalance between consumers and producers should strengthen them. We created experimental model food webs to examine the combined effects of complexity and stoichiometric imbalance on estuarine trophic cascades. A copepod, Acartia tonsa, and an aloricate ciliate, Strombidinopsis sp., served as grazers on large and small centric diatoms, Thalassiosira weissflogii and Thalassiosira pseudonana, respectively. T. weissflogii cultures were grown under nitrogen-replete and nitrogen-limited conditions, which resulted in a two-fold difference in cell carbon content and a three-fold difference in cell nitrogen content. Relative to the nitrogen-replete culture, carbon ingestion rates increased by 25% for A. tonsa and 160% for Strombidinopsis sp. fed solely on nitrogen-limited T. weissflogii (Fig. 3). However, when T. pseudonana was added to the diet of Strombidinopsis sp., the ingestion rate for T. weissflogii significantly decreased and was independent of T. weissflogii nitrogen content. A. tonsa grazed poorly on T. pseudonana, and ingestion of both nutrient replete and limited T. weissflogii increased on a mixed phytoplankton diet. For A. tonsa, the presence of the ciliate did not significantly change ingestion of T. weissflogii, regardless of phytoplankton nitrogen content. Additionally, the ingestion of ciliates by A. tonsa remained constant and proportionally small relative to phytoplankton carbon ingestion rates in all treatments. In the present study, the effects of omnivory on trophic interactions were stronger than those of stoichiometric imbalance. A similar approach to this study will be used for experiments employing toxic phytoplankton.
Fig. 3. Left panels: Copepod ingestion rate of phytoplankton versus phytoplankton with varying nitrogen content in the presence or absence of alternate food, ciliate. Right panel: Copepod ingestion rate of ciliate in the presence or absence of phytoplankton with varying nitrogen content. High and low nitrogen content in phytoplankton is denoted, respectively, by the vegetable and French fry icons. The higher nitrogen content of the ciliate is denoted by the steak icon.
Trophic cascades in contrasting ecosystems. We conducted nine experiments, along a north to south transect in the western North Atlantic (Woods Hole, Massachusetts, USA to Scarborough, Tobago), to examine planktonic trophic cascades in contrasting pelagic ecosystems. We summarized direct and indirect food web interactions in each region with models derived from path analysis, a technique that integrates correlation and multiple regression analysis. Copepods directly consumed dinoflagellates and ciliates, which resulted in positive effects on nanoplankton and bacteria. Total phytoplankton as chlorophyll a was grazed directly by copepods in New England shelf waters, but indirect (positive) effects were observed in all other regions. Indirect effects of copepod grazing were strongest in the Amazon/Orinoco plume, where 51% of the variance in bacterial growth and 81% of the variance in heterotrophic nanoplankton growth, respectively, was explained through linkages to copepods via ciliates. In the Sargasso Sea, indirect effects on bacteria via microplankton were weaker, but still evident (Fig. 4). While the complexity of food web structure superficially concealed cascading interactions, top-down effects on the lower food web were detected in all ecosystems.
Fig. 4. Illustration of indirect cascading effects of copepods on a food web. Left panel: Net growth rate of prey type versus copepod biomass. Not all prey are plotted. Numbers under the panel for each of the prey types are regression coefficients. NS = non-significant regression coefficient.
Right panel: Best fit food web model derived from path analysis. Direction of arrow indicates consumption of prey. Numbers next to arrows are path coefficients, which indicate the strength of the interaction. Width of the arrow is proportional to path coefficient. Percentages next to prey type indicate % explained variance of the prey growth rate associated with all paths leading to that prey.
Trophic Cascades and HAB. To date we have completed five trophic cascade experiments similar in scope to the nine described above, but involving the toxic dinoflagellate Alexandrium. The first two experiments used two treatments: ambient phytoplankton (presumed to be non-toxic) and ambient phytoplankton plus ~15 cells per mL of toxic A. fundyense (severe bloom in nature). Both of these experiments only revealed signifcant direct effects. A third experiment pre-exposed the copepods to toxic Alexandrium (48hrs) prior to the experiment to see if increased intoxication would lead to indirect effects. The fourth experiment used a higher dose of Alexandrium cells (150 per ml compared to 15 in previous experiments), again to see if we could induce indirect effects. We also compared non-toxic Alexandrium to toxic Alexandrium as prey in the experiments. The fifth experiment compared high and low doses of Alexandrium. We are currently analyzing the results of all five experiments (counts of chl, cells, autotrophic and heterotrophic flagellates, bacteria, etc.).
Future Activities:
In the remaining year of the grant, we plan to complete the analysis of the trophic cascades studies involving Alexandrium, conduct several trophic cascade experiments with toxic prey that test omnivory effects versus elemental imbalance of the prey, and write papers for publications.Journal Articles on this Report : 1 Displayed | Download in RIS Format
Other project views: | All 29 publications | 5 publications in selected types | All 5 journal articles |
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Type | Citation | ||
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Avery DE, Dam HG. Newly discovered reproductive phenotypes of a marine copepod reveal the costs and advantages of resistance to a toxic dinoflagellate. Limnology and Oceanography 2007;52(5):2099-2108. |
R831706 (2006) R831706 (2007) R831706 (Final) |
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Supplemental Keywords:
RFA, Scientific Discipline, Water, Ecosystem Protection/Environmental Exposure & Risk, Oceanography, algal blooms, Ecological Risk Assessment, Ecology and Ecosystems, marine ecosystem, bloom dynamics, food web, nutrient kinetics, phytoplankton, algal bloom detection, grazing and window opportunitiesProgress and Final Reports:
Original AbstractThe perspectives, information and conclusions conveyed in research project abstracts, progress reports, final reports, journal abstracts and journal publications convey the viewpoints of the principal investigator and may not represent the views and policies of ORD and EPA. Conclusions drawn by the principal investigators have not been reviewed by the Agency.