Bigelow Laboratory for Ocean Sciences

Boothbay Harbor, ME, United States

Bigelow Laboratory for Ocean Sciences

Boothbay Harbor, ME, United States
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Twining B.S.,Bigelow Laboratory for Ocean Sciences | Baines S.B.,State University of New York at Stony Brook
Annual Review of Marine Science | Year: 2013

Trace metals are required for numerous processes in phytoplankton and can influence the growth and structure of natural phytoplankton communities. The metal contents of phytoplankton reflect biochemical demands as well as environmental availability and influence the distribution of metals in the ocean. Metal quotas of natural populations can be assessed from analyses of individual cells or bulk particle assemblages or inferred from ratios of dissolved metals and macronutrients in the water column. Here, we review the available data from these approaches for temperate, equatorial, and Antarctic waters in the Pacific and Atlantic Oceans. The data show a generalized metal abundance ranking of Fe≈Zn>Mn≈Ni≈Cu≫Co≈Cd; however, there are notable differences between taxa and regions that inform our understanding of ocean metal biogeochemistry. Differences in the quotas estimated by the various techniques also provide information on metal behavior. Therefore, valuable information is lost when a single metal stoichiometry is assumed for all phytoplankton. © 2013 by Annual Reviews. All rights reserved.


Stepanauskas R.,Bigelow Laboratory for Ocean Sciences
Current Opinion in Microbiology | Year: 2012

Single cell genomics (SCG) uncovers hereditary information at the most basic level of biological organization. It is emerging as a powerful complement to cultivation-based and microbial community-focused research approaches. SCG has been instrumental in identifying metabolic features, evolutionary histories and inter-organismal interactions of the uncultured microbial groups that dominate many environments and biogeochemical cycles. The SCG approach also holds great promise in microbial microevolution studies and industrial bioprospecting. Methods for SCG consist of a series of integrated processes, beginning with the collection and preservation of environmental samples, followed by physical separation, lysis and whole genome amplification of individual cells, and culminating in genomic sequencing and the inference of encoded biological features. © 2012 Elsevier Ltd.


Grant
Agency: NSF | Branch: Standard Grant | Program: | Phase: MARINE GEOLOGY AND GEOPHYSICS | Award Amount: 522.50K | Year: 2015

Iron is one of the most abundant elements on Earth and is an essential element for life. Despite its abundance, iron is not always biologically available. For example, in the water column of the ocean, iron is easily oxidized and precipitates or sinks to the sediments. This can result in there being such a deficit of iron in the open ocean that it is often the primary limiting nutrient for the growth of phytoplankton that form the base of the marine food web. Marine sediments can be a major source of iron to the ocean, when it is made biologically available. Interestingly, one group of bacteria, the iron-oxidizing bacteria (FeOB), can use iron directly as an energy source to fuel their growth, and may govern the availability of iron to other parts of the ocean. While this group can be abundant at hydrothermal vents, little is known about their abundance or activity in marine sediments. Are these bacteria playing an important role in controlling the flux of iron from the sediments to the water column? To answer this, sediments on the east and west coasts of the United States will be analyzed to characterize and quantitate the diversity and abundance of FeOB. In addition, a series of laboratory experiments will be aimed at understanding the specific role they play in controlling iron flux from the sediments to the ocean, as well as the technically challenging question of determining the lower limit of oxygen at which they can grow. This work has relevance to our understanding of how biological control of a seemingly minor constituent in seawater, iron, could have implications for productivity of the entire ocean. Notably, a predicted impact of climate change on marine environments is to decrease oxygen levels in the ocean. This could have a profound influence on the sedimentary iron cycle, and possibly lead to greater inputs of iron, which could in turn alleviate iron-limitation in some regions of the ocean, thereby enhancing the rate of CO2-fixation and draw down of CO2 from the atmosphere. This project will provide training for a postdoctoral scientist, graduate students and undergraduates. Public outreach will include a student initiated exhibit, entitled Iron and the evolution of life on Earth at the Harvard Museum of Natural History providing a unique opportunity for undergraduate training and outreach.
The central hypothesis of this proposal is that FeOB are more common in marine sedimentary environments than previously recognized, and play a substantive role in governing the iron flux from the sediments into the water column by constraining the release of dissolved iron (dFe) from sediments. A survey of near shore regions in the Gulf of Maine, and a transect along the Monterey Canyon off the coast of California will obtain cores of sedimentary muds and look at the vertical distribution of FeOB and putative Fe-reducing bacteria using sensitive techniques to detect their presence and relative abundance. Sediments will be used in a novel reactor system that will allow for precise control of O2 levels and iron concentration to measure the dynamics of the iron cycle under different oxygen regimens. Pure cultures of FeOB with different O2 affinities will be tested in a bioreactor coupled to a highly sensitive mass spectrometer to determine the lower limits of O2 utilization for different FeOB growing on iron, thus providing mechanistic insight into their activity and distribution in low oxygen environments.


Grant
Agency: NSF | Branch: Standard Grant | Program: | Phase: | Award Amount: 745.25K | Year: 2015

Coral reefs worldwide have suffered catastrophic losses of calcifying (reef-building) organisms such as corals and crustose coralline algae (CCA). These calcifiers construct and cement the reef together, providing a complex three-dimensional structure for a diverse array of reef-associated species. On many reefs, these calcifiers have been replaced by non-calcifying, fleshy species such as seaweeds and other invertebrates. Such drastic shifts in ecosystem structure and function, documented since the 1980s, are driven by complex interactions between anthropogenically induced changes to the marine environment (i.e., eutrophication, sedimentation, or over-fishing), climate-related change (increase frequency and severity of storms, global warming, and ocean acidification), outbreaks of predators, and the spread of disease. Traditionally, investigations have largely focused on one stressor at a time, and rarely explore the complexity introduced when combinations of stressors impact a marine ecosystem, a reality most coral reefs face. This project examines an important, yet difficult to study, interaction between climate driven physical parameters (seawater temperature and pH) and the disease ecology of a coralline fungal infection, recently identified by investigators on this project, for an understudied but critical component of reef ecosystems. The primary scientific and societal broader impacts of this project will be advancing our ability to predict the future effects of climate change on disease outbreaks that negatively affect carbonate accretion and primary production of key taxa in coral reef ecosystems. This project supports the education and training of undergraduate students and a postdoctoral scholar in an international arena, engages the governors Coral Reef Advisory Group in American Samoa, and informs the general public through in-person discussions online (Google Hangout) and at a Café Scientifique.

Many tropical species of CCA are particularly sensitive to slight changes in temperature and pH in an experimental setting and the central hypothesis is that climate induced change will hasten the spread and severity of the coralline fungal disease (CFD). The exact mechanisms of how and why a previously healthy CCA host becomes infected by the endolithic fungi are unclear. Thus the two major goals of the proposed research include: 1) a description of the CFD dynamics (incidence, prevalence, and mechanism of transmission across, and progression within, various coralline host species), and 2) an exploration of how climate-driven global change (i.e., rising SST and seawater acidity) will affect these dynamics using lab experiments and field observations. A combination of high-resolution, large-scale benthic imagery and novel sensor technology arrayed across reef habitats on Palmyra Atoll will be used to relate the spatial distribution of infected or resistant host CCA species, fungal colony-forming units, and environmental conditions over time in a natural setting at a reef-scale. High frequency time series of seawater pH, pCO2, salinity, and temperature data, calibrated and complemented by discrete sampling for additional carbonate parameters (total alkalinity and dissolved inorganic carbon), will be related with biological data (disease prevalence, incidence, and host physiology). In addition, these field measurements will inform laboratory experiments performed at an organismal scale and designed to test alternative hypotheses about agents of disease progression within a calcareous host.


Grant
Agency: NSF | Branch: Standard Grant | Program: | Phase: ANTARCTIC ORGANISMS & ECOSYST | Award Amount: 1.09M | Year: 2016

The Southern Ocean in the vicinity of Antarctica is a region characterized by seasonally-driven marine phytoplankton blooms that are often dominated by microalgal species which produce large amounts of dimethylsulfoniopropionate (DMSP). DMSP can be converted to the compound dimethylsulfide (DMS) which is a molecule that can escape into the atmosphere where it is known to have strong condensation properties that are involved in regional cloud formation. Production of DMSP can influence the diversity and composition of microbial assemblages in seawater and the types and activities of microbes in the seawater will likely affect the magnitude of DMSP\DMS production. The proposal aims to examine the role of DMSP in structuring the microbial communities in Antarctic waters and how this structuring may influence DMSP cycling. The project will leverage the Antarctic research to introduce concepts and data linking microbial diversity and biogeochemistry to a range of audiences (including high school and undergraduate students in Maine). The project will also engage teacher and students in rural K-8 schools and will allow a collaboration with a science writer and illustrator who will join the team in the field. The writer will use the southern ocean experience as the setting for a poster and a book about the proposed research and the scientists studying extreme environments.

The project will examine (1) the extent to which the cycling of DMSP in southern ocean waters influences the composition and diversity of bacterial and protistan assemblages; (2) conversely, whether the composition and diversity of southern ocean protistan and bacterial assemblages influence the magnitude and rates of DMSP cycling; (3) the expression of DMSP degradation genes by marine bacteria seasonally and in response to additions of DMSP; and, to synthesize these results by quantifying (4) the microbial networks resulting from the presence of DMSP-producers and DMSP-consumers along with their predators, all involved in the cycling of DMSP in southern ocean waters. The work will be accomplished by conducting continuous growth experiments with DMSP-amended natural samples during field sampling of different microbial communities present in summer and fall. Data from the molecular (such as 16S/ 18S tag sequences, DMSP-cycle gene transcripts) and biogeochemical (such as biogenic sulfur cycling, bacterial production, microbial biomass) investigations will be integrated via network analysis.


Grant
Agency: NSF | Branch: Standard Grant | Program: | Phase: MAJOR RESEARCH INSTRUMENTATION | Award Amount: 219.26K | Year: 2016

The elements of the periodic table provide the building blocks for the earth and the organisms that inhabit it. Determining the elemental composition of organisms, along with other co-occurring environmental materials, provides valuable information for understanding basic molecular and ecological processes, determining controls on biological processes in the environment, and unraveling past environmental conditions on earth. Additionally, the elemental composition of biological and environmental samples is important information for resource managers and commercial producers. This award will fund (along with non-federal matching funds) the acquisition of a quadrupole inductively coupled plasma mass spectrometer to be used by researchers at Bigelow Laboratory for Ocean Sciences and faculty and students at nearby undergraduate colleges. The instrumentation will enable elemental measurements that will inform understanding of biogeochemical element cycling in the oceans and estuaries, as well as our knowledge of past environmental conditions and the potential response of marine species to future climate change. The instrumentation will used for both research projects and course-associated instruction for students at Bowdoin College and Colby College. Additionally, the instrumentation will provide enhanced, cutting-edge research opportunities for undergraduate students participating in Bigelow Laboratory?s on-site summer REU program and fall Changing Oceans semester program. The instrumentation will also improve research opportunities for postdoctoral researchers at the Laboratory and will enable Bigelow Laboratory to assist the local aquaculture industry with measurements of elemental composition of bivalves and macroalgae. This service will both support costs of maintaining instrumentation and enable growth of commercial output in Maine.

The award will fund purchase of a quadrupole inductively coupled plasma mass spectrometer equipped with a collision cell to reduce interferences via kinetic energy discrimination. An instrument such as the Thermo iCap Qc provides an extremely stable plasma and is capable of resolving relevant analytes such as Ti-48, Cr-52 and Fe-56. The instrument is equipped with highly efficient software, self-aligning injector, cone and lens assemblies, and fits on a benchtop. The award will also fund the purchase of an ESI seaFAST automated online sample introduction system that utilizes a resin chelation column to preconcentrate trace metal analytes of interest from seawater matrix prior to analysis.


Grant
Agency: NSF | Branch: Standard Grant | Program: | Phase: ARCTIC NATURAL SCIENCES | Award Amount: 112.40K | Year: 2016

The Arctic region has unique atmospheric chemistry leading to both positive and negative human health impacts, such as the depletion of ground-level ozone and the deposition of mercury. Atmospheric carbon dioxide uptake into sea water, moderated by the time-varying amount of sea ice cover, causes acidification of Arctic Ocean waters with potentially important impacts on the marine ecosystem. One expects that the atmosphere and its chemistry will respond in a complex manner to sea ice change and Arctic warming, but the science community lacks the ability to make predictions with confidence given only basic mechanistic understanding of the relevant processes. The O-Buoy Chemical Network project was funded under an Arctic Observing Network grant to observe atmospheric chemicals, meteorology, and sea-ice properties that can improve our understanding of the relevant processes and thus improve predictability of scenarios of future climate. That project has deployed fifteen autonomous buoys measuring three sentinel atmospheric chemical species, each for roughly a year?s time, spread across the Arctic Ocean, providing detailed, high-time-resolution data relevant to understanding the Arctic atmosphere?s chemistry in relation to sea ice. In this project, the science team will synthesize, interpret, and generate fundamental understanding from the O-Buoy network data. In addition, GEOS-Chem modeling combined with the O-Buoy measurements will be used to develop a region wide understanding of the relationship between the Arctic atmosphere and sea ice.

This project will contribute to STEM manpower development in a number of ways. It will provide support for an early career scientist during the formative years of his career. It will support the training of three Ph.D. students and engage multiple undergraduate students. Efforts will be made to draw these latter students from groups under-represented in the STEM fields by leveraging the resources of the Dartmouth College Women in Science Program (WISP) and the Alaska Native Science and Engineering Program (ANSEP) at the University of Alaska. Outreach to the K - gray community will be enabled through leveraging of existing programs such as the NSF-funded Next Generation WeatherBlur Project, the US Army Corps of Engineers Cold Regions Research and Engineering Laboratorys summer science camp for New Hampshire middle school students, the University of Alaskas annual Spring Science Potpourri open house, the weekly Café Scientifique in Boothbay Harbor, Maine: a summer lecture series that promotes public engagement with cutting-edge scientific research, and the extensive web presence of the Bigelow Laboratory for Ocean Sciences.

The Arctic Oceans overlying atmosphere is characterized by production of reactive halogen oxidizers from sea salts that lead to depletion of ground-level ozone and deposition of mercury. This production is believed to be modulated by the state of the sea ice cover. This project will answer three specific science questions relevant to the overarching question How do changes in the Arctic Ocean environment, especially sea ice, affect the atmosphere? via statistical analysis and modeling approaches. Statistical methods will test and improve process understanding while modeling approaches will be used to improve quantification of gas exchange fluxes with the Arctic Ocean through the fractured, drifting, sea ice and to predict fluxes of reactive halogen oxidizers and their precursors from sea ice. These modeling exercises make full use of the data from the O-Buoys covering the Arctic Ocean region from 2009-2016+, a period which has had a great deal of sea ice variability and reduced sea ice compared to historical averages. The three specific questions constituting the foci for this project are:
Q1: Under what conditions are carbon dioxide air-ice-ocean fluxes important causes of atmospheric carbon dioxide variability over the Arctic Ocean and, conversely, when is long-range transport important?
Q2: How do Arctic Ocean sea ice, snow, and vertical mixing conditions affect major atmospheric oxidants (ozone and reactive halogens)?
Q3: How do interannual variability and long-term declines in sea ice affect atmospheric contaminants in the Arctic?


Grant
Agency: NSF | Branch: Standard Grant | Program: | Phase: ARCTIC NATURAL SCIENCES | Award Amount: 108.95K | Year: 2016

The highly productive and economically important Walleye Pollock commercial fishery of the Bering Sea depends on poorly understood food web pathways. Primary producers of organic carbon, notably diatoms, are consumed by large crustacean zooplankton, which, in turn, are consumed by juvenile pollock. The dominant paradigm for the system suggests that understanding changes in the biomass of large crustacean zooplankton can help estimate the survival of juvenile pollock; however, recent data show two orders of magnitude uncertainty in the carbon demand of large crustacean zooplankton. Such uncertainties impact the ability to manage the fishery. A revised model for the system has been proposed that involves consideration of both the quantity and quality of organic matter produced by diatoms and how this would constrain support for the commercial fishery. Before investing in a major field effort to test this approach, this project will assess the expected magnitude of change and associated errors, for diatom organic matter production, including the individual terms that are used to estimate it, i.e. abundance, growth rate, and cell carbon. This effort will be based on laboratory experiments and historical data analysis.

The project will contribute to STEM workforce development through partial support for the training of a post-doctoral associate. Undergraduates would be entrained into the science through an REU program at Bigelow Laboratory for Ocean Sciences and through the Colby College Semester at Bigelow program. K-12 outreach will be facilitated through participation in the successful and long-standing Dauphin Island Sea Lab Discovery Hall program. Outreach to the general public will be accomplished through a blog, Bigelow?s Café Scientifique, and the Bigelow newsletter. The long-term goal for the research that this project would initiate is improved mechanistic and predictive models for commercial fisheries management.

There is no consensus on the mechanistic relationship of where carbon from the lower trophic levels goes in the Bering Sea ecosystem, hence simple proportionality relationships between primary production and fisheries are used routinely. Bottom-up control on age-0 walleye pollock prey, i.e. large crustacean zooplankton (LCZ), could help constrain this coupling between the primary producers and pollock fishery, but there is a two-order-of-magnitude uncertainty in the LCZ carbon demand based on estimates from the Bering Sea Ecosystem Study (BEST). A new conceptual model is required and this project will begin to refine the issue by focusing on diatoms, which have a less patchy distribution than LCZ and are a key prey item of LCZ. A major knowledge gap exists in the understanding of the magnitude of diatom loss processes; the logical next step to understanding the fundamental linkage between primary production and fisheries in the eastern Bering Sea is to answer: what is the proportion of diatom primary production available for supporting higher trophic organisms and with which biogeochemical variables does this covary? Before testing this approach in a field setting, the expected magnitude of change and associated error for diatom organic matter production, including the individual terms that go into that estimate (i.e. abundance, growth rate, cell carbon), must be understood. This project will combine culture studies using diatoms isolated from high-latitude regions with literature and BEST program data to meet this initial objective.


Grant
Agency: NSF | Branch: Standard Grant | Program: | Phase: BIOLOGICAL OCEANOGRAPHY | Award Amount: 319.66K | Year: 2016

The Indian Ocean accounts for nearly a fifth of global ocean photosynthesis and is likely a key component in global ocean nutrient and carbon cycles. However, the Indian Ocean may be the least studied major marine body on the planet. Our limited understanding suggests extensive variations in physical and chemical environmental conditions, but how this variation influences biodiversity, nutrient stress, and more broadly regional differences in the functioning of phytoplankton is unknown. To help address these gaps, the investigators will conduct a study by joining an already-funded major research cruise to this region. It will cover a northern region with some of the highest temperatures recorded in open ocean waters, an area around 10°S of predicted (but not tested in situ) iron stress, and a southern subtropical gyre with unique nitrogen to phosphorous(or N:P) ratios. The focus of this project is to quantify and synthesize the interconnectedness of environmental conditions, phytoplankton diversity and genome content, and nutrient biogeochemistry, with the goal of understanding how these may lead to unique biogeochemical regions in Indian Ocean. The research will have broader impacts on many levels. First, it will increase public awareness of the role of phytoplankton on ocean functioning, climate, and peoples lives through a new partnership with the Aquarium of the Pacific (AOP), which is the fourth most-attended aquarium in the nation. Secondly, the project will train a postdoctoral scholar as well as a graduate and undergraduate students. Third, the research will dramatically increase our basic knowledge ocean biogeochemistry and in many cases will be the first measurements of their kind made in the Indian Ocean.

This project will address two major questions: How do environmental conditions, phytoplankton diversity, phytoplankton physiology, and biogeochemistry vary across the central Indian Ocean? Are there distinct biogeochemical regimes in the central IO? The researchers hypothesize that environmental conditions, including the relative availability of nitrogen (N) and iron (Fe), lead to three distinct phytoplankton communities and biogeochemical regimes. They will employ a series of advanced analytical tools including high sensitivity measurements of dissolved and particulate nutrients (nitrogen, phosphorus, and iron), genomics, bioassays to test for nutrient stress, and cell-sorting of specific taxa followed by measures of nutrient content and uptake. A focus of this project is to quantify and synthesize the interconnectedness of environmental conditions, phytoplankton diversity and genome content, and nutrient biogeochemistry, and how these lead to unique biogeochemical regions in Indian Ocean. This extensive set of observations can ultimately be linked to ocean models and satellite data to provide a comprehensive view of regional differences in chemistry, biodiversity and phytoplankton biogeochemical functioning in the Indian Ocean.


Grant
Agency: NSF | Branch: Standard Grant | Program: | Phase: BIOLOGICAL OCEANOGRAPHY | Award Amount: 669.75K | Year: 2016

Coccolithophores are single-cell algae that are covered with limestone (calcite) plates called coccoliths. They may make up most of the phytoplankton biomass in the oceans. Coccolithophores are generally considered to be autotrophs, meaning that they use photosynthesis to fix carbon into both soft plant tissue and hard minerogenic calcite, using sunlight as an energy source (autotrophic). However, there is an increasing body of evidence that coccolithophores are mixotrophic, meaning that they can fix carbon from photosynthesis as well as grow in darkness by engulfing small organic particles plus taking up other simple carbon molecules from seawater. The extent to which Coccolithophores engage in mixotrophic can influence the transfer of carbon into the deep sea. This work is fundamentally directed at quantifying coccolithophore mixotrophy -- the ability to use dissolved and reduce carbon compounds for energy -- using lab and field experiments plus clarifying its relevance to ocean biology and chemistry. This work will generate broader impacts in three areas: 1) Undergraduate training: Two REU undergraduates will be trained during the project. The student in the second year will participate in the research cruise. 2) Café Scientifique program: This work will be presented in Bigelow Laboratory?s Café Scientifique program. These are free public gatherings where the public is invited to join in a conversation about the latest ideas and issues in ocean science and technology. 3) Digital E-Book: We propose to make a digital E-book to specifically highlight and explain mixotrophy within coccolithophores. Images of mixotrophic coccolithophores would be the primary visual elements of the book. The E-book will be publically available and distributed to our educational affiliate, Colby College. The goal of the book is to further communicate the intricacies of the microbial world, food web dynamics, plus their relationship to the global carbon cycle, to inspire interest, education, and curiosity about these amazing life forms.

Coccolithophores can significantly affect the draw-down of atmospheric CO2 and they can transfer CO2 from the surface ocean and sequester it in the deep sea via two carbon pump mechanisms: (1) The alkalinity pump (also known as the calcium carbonate pump), where coccolithophores in the surface ocean take up dissolved inorganic carbon (DIC; primarily a form called bicarbonate, a major constituent of ocean alkalinity). They convert half to CO2, which is either fixed as plant biomass or released as the gas, and half is synthesized into their mineral coccoliths. Thus, coccolithophore calcification can actually increase surface CO2 on short time scales (i.e. weeks). However, over months to years, coccoliths sink below thousands of meters, where they dissolve and release bicarbonate back into deep water. Thus, sinking coccoliths essentially pump bicarbonate alkalinity from surface to deep waters, where that carbon remains isolated in the abyssal depths for thousands of years. (2) The biological pump, where the ballasting effect of the dense limestone coccoliths speeds the sinking of organic, soft-tissue debris (particulate organic carbon or POC), essentially pumping this soft carbon tissue to depth. The biological pump ultimately decreases surface CO2. The soft-tissue and alkalinity pumps reinforce each other in maintaining a vertical gradient in DIC (more down deep than at the surface) but they oppose each other in terms of the air-sea exchange of CO2. Thus, the net effect of coccolithophores on atmospheric CO2 depends on the balance of their CO2-raising effect associated with the alkalinity pump and their CO2-lowering effect associated with the soft-tissue biological pump. It is virtually always assumed that coccolith particulate organic carbon (PIC) originates exclusively from dissolved organic carbon (DIC, as bicarbonate), not dissolved organic carbon (DOC). The goal of this proposal is to describe a) the potential uptake and assimilation of an array of DOC compounds by coccolithophores, b) the rates of uptake, and potential incorporation of DOC by coccolithophores into PIC coccoliths, which, if true, would represent a major shift in the alkalinity pump paradigm. This work is fundamentally directed at quantifying coccolithophore mixotrophy using lab and field experiments plus clarifying its relevance to ocean biology and chemistry. There have been a number of technological advances to address this issue, all of which will be applied in this work. The investigators will: (a) screen coccolithophore cultures for the uptake and assimilation of a large array of DOC molecules, (b) perform tracer experiments with specific DOC molecules in order to examine uptake at environmentally-realistic concentrations, (c) measure fixation of DOC into organic tissue, separate from that fixed into PIC coccoliths, (d) separate coccolithophores from other phytoplankton and bacteria using flow cytometry and e) distinguish the modes of nutrition in these sorted coccolithophore cells. This work will fundamentally advance the state of knowledge of coccolithophore mixotrophy in the sea and address the balance of carbon that coccolithophores derived from autotrophic versus heterotrophic sources.

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