EPA 600/3 78-025
February 1978
Ecological Research Series
PHYTOPLANKTON SAMPLING IN QUANTITATIVE
BASELINE AND MONITORING PROGRAMS
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RESEARCH REPORTING SERIES
Research reports of the Office of Research and Development, U.S. Environmental
Protection Agency, have been grouped into nine series. These nine broad cate-
gories were established to facilitate further development and application of en-
vironmental technology. Elimination of traditional grouping was consciously
planned to foster technology transfer and a maximum interface in related fields.
The nine series are:
1. Environmental Health Effects Research
2. Environmental Protection Technology
3. Ecological Research
4. Environmental Monitoring
5. Socioeconomic Environmental Studies
6. Scientific and Technical Assessment Reports (STAR)
7. Interagency Energy-Environment Research and Development
8. "Special" Reports
9. Miscellaneous Reports
This report has been assigned to the ECOLOGICAL RESEARCH series. This series
describes research on the effects of pollution on humans, plant and animal spe-
cies, and materials. Problems are assessed for their long- and short-term influ-
ences. Investigations include formation, transport, and pathway studies to deter-
mine the fate of pollutants and their effects. This work provides the technical basis
for setting standards to minimize undesirable changes in living organisms in the
aquatic, terrestrial, and atmospheric environments.
This document is available to the public through the National Technical Informa-
tion Service, Springfield, Virginia 22161.
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EPA-600/3-78-025
February 1978
PHYTOPLANKTON SAMPLING IN QUANTITATIVE
BASELINE AND MONITORING PROGRAMS1/
by
Paul E. Stofan and George C. Grant
Virginia Institute of Marine Science
Gloucester Point, Virginia 23062
Grant Number -
EPA-R804147010
Project Officer
Richard C. Swartz
Newport Field Station
Marine and Freshwater Ecology Branch
Corvallis Environmental Research Laboratory
Newport, Oregon 97365
CORVALLIS ENVIRONMENTAL RESEARCH LABORATORY
OFFICE OF RESEARCH AND DEVELOPMENT
U. S. ENVIRONMENTAL PROTECTION AGENCY
CORVALLIS, OREGON 97330
' Special Scientific Report No. 85, Virginia Institute of Marine Science
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DISCLAIMER
This report has been reviewed by the Corvallis Environmental Research
Laboratory, U.S. Environmental Protection Agency, and approved for publi-
cation. Approval does not signify that the contents necessarily reflect
the views and policies of the U.S. Environmental Protection Agency, nor
does mention of trade names or commercial products constituted endorsement
or recommendation for use.
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FOREWORD
Effective regulatory and enforcement actions by the Environmental Protection
Agency would be virtually impossible without sound scientific data on pollu-
tants and their impact on environmental stability and human health. Respon-
sibility for building this data base has been assigned to EPA's Office of
Research and Development and its 15 major field installations, one of which
is the Corvallis Environmental Research Laboratory (CERL).
The primary mission of the Corvallis Laboratory is research on the effects
of environmental pollutants on terrestrial, freshwater, and marine ecosystems;
the behavior, effects and control of pollutants in lake systems; and the
development of predictive models on the movement of pollutants in the
biosphere.
This report presents a review of methods for sampling and analyzing marine
phytoplankton communities. These quantitative techniques can be used to
establish ecological baselines or to conduct surveys of the impact of pol-
lution on phytoplankton dynamics.
A. F. Bartsch
Director, CERL
iii
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ABSTRACT
An overview of phytoplankton sampling and analysis methods as they apply to
quantitative baseline and monitoring surveys is provided. A need for in-
clusion of a preliminary field survey of the area under investigation and
of flexibility in sampling design is stressed. An extensive bibliography
pertinent to phytoplankton sampling and analysis is included in the report.
This report was submitted in fulfillment of Contract No. R804147010 by the
Virginia Institute of Marine Science under the sponsorship pf the U. S.
Environmental Protection Agency. This report covers a period from 24 Nov
75 to 31 May 77, and work was completed as of 15 Sept 77.
iv
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CONTENTS
Foreword
Abstract
Contents
. Acknowledgments
Sections
1 Conclusions 2.
2 Introduction o
3 Phytoplankton Ecology ^
4 Sampling Design for Environmental Assessment 7
4.1 Oceanic Sampling 7
4.2 Estuarine Sampling 7
5 Phytoplankton Vertical Heterogeneity 9
5.1 Surface Microlayer Sampling g
5.2 Subsurface Sampling IQ
5.3 Aphotic Zone Sampling n
6 Sample Treatment 12
6.1 Sample Volume ^2
6.2 Live Sample Analysis ^2
6.3 Sample Fixation ^3
7 Sample Concentration ^5
7.1 Settling 15
7.2 Centrifugation 15
7.3 Filtration 15
8 Phytoplankton Enumeration 17
8.1 Utermohl Method 17
8.2 Conventional Counting Methods 18
8.3 Particle Counters 18
8.4 Fluorescence Microscopy 18
9 Primary Productivity 20
v
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Sections
10 Phytopigment Fluorescence 21
11 Solar Radiation 22
12 Ancillary Hydrography 23
13 Statistical Considerations 24
14 References 25
Literature Cited 25
Selected Ecological Bibliography 38
Phytoplankton Survey and Distribution Bibliography 46
Phytoplankton Methodology Bibliography 60
Phytoplankton Identification Bibliography 70
Selected Statistical Bibliography 77
VI
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ACKNOWLEDGMENTS
Dr. Richard Swartz of the Environmental Protection Agency was instrumental
in the plan to prepare a procedural guide for quantitative phytoplankton
analyses in baseline monitoring programs. He provided encouragement, support
and guidance during the preparation of this report.
Thanks and appreciation are extended to Arlene Rosenbaum for reviewing the
drafts of this report and for providing constructive criticism. Thanks are
due to Ruth Edwards for her patient typing and retyping of this report, and
to Shirley Sterling for typing the final draft.
vii
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SECTION 1
CONCLUSIONS
The complexity of dynamic oceanic and estuarine ecosystems prevent the
preparation of a detailed and concise survey outline. The current status
of phytoplankton surveys was determined through searches of data storage
banks, National Oceanographic Data Center (NODC), Biological Abstracts (BA),
Biological Information Retrieval System (BIRS), Bioresearch Index (BRI),
Ocean Abstracts (OA), Selected Water Resources Abstracts (SWRA), Smithsonian
Science Information Exchange (SSIE) and Environmental Data Index (ENDEX).
The results of these searches illustrated the need for survey design flex-
ibility to accommodate the array of phytoplankton investigative procedures.
The wide selection of methodology has arisen from complexities within the
marine ecosystems. The development of a specific survey design is directly
a function of both the character of the marine system to be surveyed and
the purposes for developing the survey. However, some general recommenda-
tions can be made.
The early developmental stages of a survey design are considered crucial,
since appropriate planning is necessary to develop a general understanding
of the anticipated complexities of the system under consideration. The
selection of station locations and sampling frequency can dramatically
influence the statistical validity of the obtained information. Where
applicable, the investigative area should be divided into its discernible
hydrographic sub-areas. These sub-areas should be overlaid with a grid,
which provides a statistically valid basis for sampling within each sub-
area. The sampling frequency must be short enough to reveal major temporal
community changes. The frequency of sampling in an estuarine system should
be biweekly or monthly during periods of relatively stable environmental
conditions and weekly during periods of hydrographic instability. Because
oceanic hydrography changes less rapidly, the sampling may vary from bi-
monthly to biweekly. Any perturbation of the ecosystem should be followed
by intensified sampling to ascertain the resultant community alterations.
The selection of sampling devices and depths is largely dependent on the
nature of the desired information. Generally, sub-surface bottle sampling
is most efficient in eutrophic waters having high phytoplankton densities,
while net or pump sampling may be desired for oligotrophic oceanic regions.
A survey is not complete without delineation of phytoplankton vertical
heterogeneity and its analysis. The screen sampler is well suited for
surface sampling. The deployment of a skiff at sea is often discouraged
but is the only reliable method of avoiding the "hull-effect" of a larger
vessel. A significantly less satisfactory surface sampler is the modified
Zaitsev neuston net.
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Enumeration procedures must be carefully considered because each method has
its own intrinsic deficiencies and the Utermohl method appears to be the most
generally used and accepted procedure because it provides a wide range of
adaptability at medium cost. Conventional live analysis should be simultane-
ously performed on sample aliquots.
The analysis of phytoplankton in a general baseline survey should be accom-
panied by a wide array of ancillary data. These data include the delineation
of zooplankton, ichthyoplankton and benthic communities, in addition to
standard hydrographic analyses. The Carbon -^ productivity estimate is the
most widely used and whenever possible should be included in baseline
surveys. Chlorophyll a_ estimates of standing stock may yield pertinent
correlative information with identification, enumeration and productivity
measurements and, thereby, contribute to a comprehensive phytoplankton
community survey.
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SECTION 2
INTRODUCTION
Baseline and monitoring surveys of estuarine, coastal and oceanic waters have
been widely employed as a means of obtaining biological and ancillary data
needed in assessing environmental impacts of various human activities. The
size, cost and comprehensiveness of these surveys vary with the type of action
and the expected impact, e.g. from small, localized additions of effluent to
development of a major offshore oil field. Such surveys originate in response
to enacted law, requiring that industry provide an environmental assessment
before and after an event of perturbation so as to protect the public. The
scientists charged with designing and carrying out these surveys are respon-
sible, therefore, for assuring that meaningful data are collected in a manner
that will allow pertinent assessment of environmental changes. The cost must
be held to a level commensurate with the probable impact, and all needed
observations should be taken.
Measurements and observations included in baseline surveys are usually similar
but may vary somewhat with the type of environmental alteration.under consid-
eration, e.g. emphasis on hydrocarbon measurements in offshore oil fields,
benthic organisms and turbidity in channel dredging, or mortality of fish
eggs and larvae in power plant installations. Most surveys include standard
hydrographic observations, an inclusion of lower trophic levels, and studies
of the benthos and fishes. Somewhat surprising is the omission of phyto-
plankton studies from many of the major baseline surveys. In view of their
critical role in the food web and productivity of marine waters and of their
rapid response to environmental perturbations, phytoplankton should certainly
be included in any survey designed to measure environmental impact. It is
our experience that omission of phytoplankton studies from broad baseline
surveys is usually a result of the inability of phytoplanktologists to agree
on what constitutes meaningful observations.
This report is intended as an overview of methods used for phytoplankton
sampling, sample treatment and analysis. It is also intended primarily for
the agency personnel requesting proposals and the survey designer, rather
than for practicing phytoplanktologists.
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SECTION 3
PHYTOPLANKTON ECOLOGY
An accurate evaluation of the phytoplankton community in any given body of
water requires an extensive knowledge of general phytoplankton biology and
ecology. The following brief perusal of some of the major considerations
is intended to provide insight into this dynamic system and thereby aid the
researcher in both the design of an investigation and the evaluation of
obtained data.
The role of phytoplankton in the marine and estuarine environment is essen-
tially the capture of radiant energy and the metabolic concentration of
dissolved inorganic chemicals. The cell uses the captured radiant energy
to combine the inorganics, through photometabolism, into complex organic
molecules.1~2 These molecules are then used in cellular maintenance, growth,
and reproduction. The phytoplankton community is the principal producer in
the world's oceans and thus it serves as the major energy source for higher
marine trophic levels. Furthermore, numerous secondary influences are
produced by phytoplankton induced alterations of the aquatic environment.^
These include uptake of carbon dioxide and the release of oxygen during
periods of photometabolism. Phytoplankton were historically instrumental
in the stabilization of oxygen in the atmosphere and thereby provided the
aerobic environment of consumers. Waste products and other metabolites
released by phytoplankton can act as regulatory agents in the succession
of species. Although usually unobserved, these agents occasionally produce
pronounced effects as evidenced by red tides. ~° Additionally, the excretion
products and dead cells are functional in the determination and maintenance
of the heterotrophic community.'
Limiting and controlling factors on the phytoplankton community generally
include the availability of nutrients, solar radiation, salinity and temper-
ature. 8-17 The activities of man have clearly altered these factors in the
continental inland waters and estuaries. In addition, biotic changes on the
continental shelf have been observed, as evidenced by the summer 1976, east
coast bloom of Ceratium tripos. The decline of this bloom and its associated
oxygen deficit resulted in massive finfish and shellfish mortality.1®
The addition of inorganic and organic c:ompounds from effluents and run-off
stimulates phytoplankton growth whereas the addition of toxic compounds like
DDT, PCB, PBB and Kepone may limit growth.19"20 Excessive phytoplankton
growth is usually observed as a logarithmic population increase of a very few
algal species. These species completely dominate the community until some
environmental factor becomes limiting. The bloom species may not be directly
toxic as with the red tide dinoflagellates, but may produce secondary effects,
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including radically fluctuating oxygen levels between light periods of photo-
metabolism and dark periods of respiration. Bloom species may have a delete-
rious effect on filter-feeding consumers by radically reducing the abundance
of more desirable phytoplankton species selectively filtered as foodstuffs.
The addition of trace amounts of toxic compounds to the aquatic system often,
through bio-concentration mechanisms, results in highly toxic levels in the
tissues of the entire associated food web. The mechanisms for the degree of
bio-concentration by the algae vary with each compound and with each species.
An accurate assessment of the phytoplankton community also requires an under-
standing of the spatial and temporal characteristics of algae. " Spa-
tially, the phytoplankton inhabit a three-dimensional world with accordingly
complex distributional anomalies. Vertically the organisms may stratify into
a surface community occupying the surface film and immediate underlying
waters, a near surface community from one to approximately ten meters deep,
a deep community near the compensation depth, as well as an aphotic zone
community. The exact number of identifiable communities and their depth will
vary in accordance with incident light, turbidity, vertical mixing and with
the phytoplankton species occupying the water mass. Horizontal heterogeneity
has long been observed in the patchiness of visual blooms. Windrows and
down-wellings often increase cell densities of certain locations while
decreasing them in the adjacent water. Patches or high density communities
vary from only a few meters in width to many miles. Spatial heterogeneity
is further complicated by the movements of the water. Currents are usually
relatively stable in oceanic environments, more complex in continental shelf
and slope waters, and often highly complicated in estuaries. Rarely is the
researcher able to use a simple up-stream down-stream approach and is, there-
fore, required to know, either through the literature or through measurement,
the circulation patterns to be encountered in the region under study.
In addition to observed spatial variations, temporal changes in the phyto-
plankton density and species composition must be anticipated. Seasonally the
communities will proceed through compositional changes in a fairly predictable
manner, the primary influencing factors usually being temperature, incident
radiation, nutrients and salinity. "~33 ^g particular seasonal pattern for
a given water mass or area must be determined through seasonal sampling.
Fluctuations within a community may occur slowly, requiring a month or more,
or may be very abrupt, occurring in a week or less.^ Once the seasonal
pattern has been determined, its changes are then often predictable from
knowledge of the hydrography of the water.
Sampling of the phytoplankton communities is therefore complicated by both
vertical and horizontal patchiness, and abrupt or slow seasonal changes, in
addition to water circulation patterns, grazing, circadian migration and
radiation fluctuations.
The dynamics of the marine aquatic environments are so variable that sample
design should be flexible, allowing adaptation to observed peculiarities of
the system under investigation. The open seas with their relatively uniform
hydrography provide an area suitable for observation and description of
circadian patterns. Drogue buoys can be employed to identify water mass
movements and allow repeated sampling from the same communities. In contrast,
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the estuarine system, each with its unique form of heterogeneity, presents
extreme problems of relating replicated and sequential samples. In attempting
any circadian investigations in an estuary, a prime consideration is deter-
mining what water mass is being sampled and at what time. The significance
of the circadian pattern at a point location has not been accurately compared
with the circadian pattern of a discreet water parcel. Also, the problems of
dissimilarity of replicate samples in the estuary is more pronounced than
that encountered in oceanic replication. It is evident that the more heter-
geneous and dynamic a system, the greater the problems are in accurately
delineating the biotic events.
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SECTION 4
SAMPLING DESIGN FOR ENVIRONMENTAL ASSESSMENT
The location and number of stations and the depths to be sampled determines
both the value and the cost of the obtained information. The primary consid-
eration in a sampling scheme should be to obtain the amount of information
about the phytoplankton community required to answer the questions of inves-
tigators. The correct framing of these questions is thus of the utmost
importance to all that follows. An investigation of the literature pertinent
to the general area and a detailed preliminary field sampling can often result
in a reduction of samples required. It is desirable to determine the charac-
teristic annual cycles and the distributional patterns in the first year or
two of sampling. Once these patterns are determined with the accompanying
hydrography, sampling can then be reduced to a monitoring basis. The impor-
tant preliminary field sampling has often been neglected because most in-
vestigative work is limited to a fixed number of stations and samples pre-
determined by budgetary limitations.
4.1 Oceanic Sampling
For a proposed investigation of the continental shelf or slope, the locations
and characteristics of the water masses can usually be determined from pub-
lished studies on hydrography, current analysis, and biotic community anal-
ysis. The neritic, near-shore waters are usually clearly discernible from
deeper shelf waters and oceanic waters. Charts of the sub-areas should be
marked with a grid and random sampling should be performed within each sub-
area. This type of sampling scheme provides the most statistically valid
description of the communities within each sub-area. Seasonal station
replication is not completely relevant since the water masses are in a
state of continuous dynamic fluctuation.28,35-40 jn situations where results
of an investigation are to be correlated with other biotic and hydrographic
data, it may be necessary to sample on a fixed station scheme. This is often
the case with inlet and discharge monitoring or when sampling is coupled with
more stationary benthic community analysis. In selecting such fixed stations
it is essential to locate them within each of the above mentioned sub-areas.
The specific station locations within each sub-area should sample each
micro-climate or each recognizable water type of that sub-area. Because
of the high costs of offshore operations, it is customary to locate stations
along transects to reduce the between-station time and thereby reduce the
cost per sample.
4.2 Estuarine Sampling
For an investigation in an estuary the problems of station location are
7
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similar to those in the offshore environment. However, both spatial and
temporal changes become more pronounced within the estuarine environment.
Water movement becomes highly complicated due to interactions of tidal
currents with seasonally fluctuating upstream fresh water discharge, in
addition to the wind driven currents and mixing. The complexity in the
composition of estuarine waters is increased by the input of agricultural,
industrial and domestic impurities. As the chemical and silt laden fresh
water mixes with the high saline tidal input, a wide range of temperatures,
nutrients and salinities may be encountered over very short distances.
Accordingly, estuarine investigations should be one of two types. A gen-
eral evaluation of the entire estuary requires dividing the estuary into
basic hydrographic strata followed by multiple sampling within each stratum.
The number of samples needed in each stratum should be determined from
variations observed in the preliminary field study. Such a sampling scheme
resembles that described for the shelf and slope investigative procedures.
The alternative sampling scheme is appropriate for an estuarine system with
a specific localized environmental problem. The investigation is usually
associated with answering specific questions of water quality alteration
from some land-based operational discharge. This entails.the delineation
of the phytoplankton communities prior to the construction and operation
of the discharge and a monitoring program after the installation. The degree
of detail in the sampling scheme is directly dependent on the magnitude of
the proposed discharge and its subsequent extent of alteration of hydrography
and biology.
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SECTION 5
PHYTOPLANKTON VERTICAL HETEROGENEITY
Once the stations have been selected it is necessary to determine the degree
of specificity that the investigation requires. This is a major determinant
of the number of samples to be collected at each station, the various types
of collecting apparatus to be utilized, and the resultant cost of the study.
If a general water quality investigation is required, it is necessary to
sample the vertically stratified communities: surface micro-layer, near-
surface photic zone, compensation depth and aphotic zone. These depths should
reveal what complexities will be encountered at each station and between
stations.
5.1 Surface Microlayer Sampling
The surface micro-layer is efficiently sampled with the Garrett-type screen
sampler. 1-^2 The frame and screen should be constructed of some non-toxic
non-contaminating substance if the samples are to be used for anything other
than identification and enumeration of the phytoplankton. The samples should
be taken well away from the hull of any large ship, in relatively undisturbed
water. The surface microlayer community has been found to maintain its
integrity in wind-driven waves of one meter.^3 if the waves are strongly
cresting the community has probably mixed with the near surface community
and a gradient from one to the other would exist.
The screen sampler should be horizontally submerged, moved to an adjacent
undisturbed area, and slowly lifted up through the surface waters while
keeping it in the horizontal position.42 The screen is then tilted so that
the adhered water will drain from one corner of the screen until only a slow
drip remains. The procedure is repeated until the desired volume of surface
water has been collected. A two (2) foot square screen will generally yield
approximately 75-100 mrlliliters per submergence. Large mouth plastic
funnels and bottles are recommended for use at sea to reduce the danger
of breakage and the loss of samples. Sample size generally should be in
excess of the 1000 milliliters used for settling (see 6.0 sample treatment).
Alternate surface micro-layer sampling includes the glass plate method of
removing the surface adhesion layer and use of the Harvey drum type sampler.
Both of these methods are most applicable in very calm waters. A
modified Zaitsev neuston net could be used to sample various near surface
layers and the. surface sub-surface ecotone.46-47
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5.2 Subsurface Sampling
Sampling of the near surface, compensation depth, and aphotic communities
can be investigated from three different methodological approaches, yielding
different evaluations.22'48"51 Discreet depths can most accurately be
sampled with any of various bottle or pump samplers. There are no standard
sampling depths because of the variable vertical distributions of the phyto-
plankton. The exact depths to be sampled should be established by consulting
previous studies of the research area together with a preliminary sampling of
hydrographic and biotic profiles. A less sophisticated approach is to pre-
select arbitrary depths throughout the water column. This approach may
result in an unnecessarily large number of samples to be analyzed. In tropic
and sub-tropic oceanic waters, pre-selected depths should include the sur-
face, near surface, 10, 25, 50, 75, 100, 150 and 200 meter depths. Temperate
and boreal waters, typically more productive, require closer spacing of the
samples: surface, near surface, 5, 10, 20, 40, 60, 80 and 100 meter depths.
Coastal waters, estuaries and upwelling support denser phytoplankton commun-
ities and may require even closer spacing of sample depths: surface, 1.5,
3, 5, 10, 20, 40 and 60 meters.
Endogenous diurnal rhythms of phytoplankton photosynthesis, nutrient uptake,
cellular maintenance, growth and reproduction, often result in vertical
circadian migrations. The migration patterns have been amply demonstrated
for many species and the net effect of these migrations may significantly
distort results unless the time of sampling is accounted for. The time and
magnitude of these circadian movements are species specific and may result
from both positive and negative stimuli. Sampling for general survey infor-
mation should usually be conducted between dawn and dusk; mid-morning and
mid-afternoon are the more preferable times.
Migrations are generally believed to be a response to ambient light intensity.
This theory accounts for depressed productivity values around noon. Recent
demonstrations of a discrete surface microlayer phytoplankton community has
elicited reconsiderations of light inhibition theories and may ultimately aid
in clarifying migration related problems.
A thirty (30) liter Niskin bottle fitted with a large bore spigot provides
accurate samples in both volume and depth and is most appropriate for off-
shore oligotrophic waters.52 A sample can be immediately run through a ten
(10) or twenty (20) micron sieve and then resuspended and preserved in 250
milliliter bottles. The closing bottle samplers have proved to be the most
easily used quantitative sampling devices. A wide range of designs have
been developed for specific applications. Generally, the samplers should
have a streamlined flow-through design with no corners or areas to trap and
hold residual water while being moved to the desired depth. Such a feature
is mot important when sampling very small phytoplankton, fungi and bacteria.
Bottle construction should be of non-contaminating materials because samples
are often split into aliquots for various ancillary analyses. The bottles
should be designed to be used in series enabling sequential closing. Spe-
cially designed samplers have been developed for the elimination of
contamination.
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A bottle type sample does not account for the microdistributional anomalies
so frequently encountered in phytoplankton communities. Repeated sampling
at a given depth using a smaller volume bottle will provide an approximation
of an integrated sample. When patchiness is a concern, an integrative sampler
should be considered. Discreet depth integration can also be accomplished
using a pump to bring the water to the surface-^"-1' Various types of pumping
systems have been employed since the late 19th century. The discharge can be
run through a sieve for concentration and the filtrate collected until any
desired volume has been filtered. The filtrate may be used to wash the phyto-
plankton from the sieve. The rate of flow in the hose and pump must be con-
trolled to keep the cells from adhering to the surfaces and to keep cell
damage to a minimum. An alternate and less desirable method of integrative
sampling is to use a vertical or oblique net tow. Both types of net tows
integrate not only the horizontally micro-distributed phytoplankters but
also integrate the vertically stratified communities. Furthermore, there
is no accurate method of determining the amount of water filtered through
fine-meshed nets; only gross quantitative approximations of the population
densities can be made. Dense zooplankton communities further compound the
problems of quantification by clogging fine meshed nets, terminating or
reducing filtration efficiency. Ctenophora, jellyfish and salps add to the
difficulty by entangling organisms within a mass of tentacles and jelly, thus
making samples unmanageable. However, net tows can be useful in providing
large numbers of cells for morphological and taxonomic studies.
Various modifications of net type continuous samplers have been designed.->°~
"1 Generally, they provide a continuous sample while being towed through
the water. A small aperture allows a stream of water to be filtered through
a spool mounted net. The netted phytoplankton are automatically preserved in
place on the net for later microscopic analysis. The continuous samples are
useful in determining the horizontal distribution of phytoplankton communi-
ties over large areas of ocean. This type of sampling device has a variable
spool speed which can be adjusted in accordance to the plankton density and
thereby has application in both oligotrophic and eutrophic waters.
5.3 Aphotic Zone Sampling
Viable deep-water phytoplankton have frequently been reported from deep
oceanic waters. The grouping of these phytoplankton as a community is still
under investigation. *>z Bottle-sampling of aphotic zone phytoplankton should
proceed with preliminary sampling at predetermined depths between the bottom
and the compensation depth. Phytoplankton concentrations often correlate
with inflection points of temperature and salinity, which are usually in-
dicative of boundaries between different water masses. Immediate live
sample analysis may establish the presence of aphotic phytoplankton and
define their approximate vertical position so that an intensive samplirfg
array may be initiated at such locations.
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SECTION 6
SAMPLE TREATMENT
Nearly all samples require some form of concentration prior to enumeration.
The enumerative method to be used usually involves its own particular man-
ipulative procedures. Early decisions include the volume of sample to be
enumerated, the number of aliquots necessary for accurate subsampling, and
the number of replicate counts to assure an accurate estimate of the actual
community. The wide range of cell densities and the abundance of partic--
ulate detrital material make general recommendations for sample volumes
inadvisable. Additional factors which must be considered include the size
range of the community components, the resultant magnification requirements
for their positive identification, the dispersal characteristics of the
selected counting chambers, the minimum numbers of cells needed for satis-
factory abundance estimates, and for assured observation of the rare and
moderately rare species. Each counting method has pertinent publications
dealing with its own unique statistical considerations. The complexities
of these problems are illustrated by comparisons between various aliquot
sizes and the resultant disproportionate changes within the various phyto-
plankton groups. A number of these methods are discussed in section 8.0
phytoplankton enumeration.
6.1 Sample Volume
The required sample volume will vary with the type of sampling gear employed,
the type of analysis to be performed, and the density of the phytoplankton
community. The most important consideration is cell density, which may range
from only a few cells per liter in oligotrophic oceanic waters to a billion
or more cells per liter in estuarine bloom conditions. A field estimate of
cell densities is often the most effective means of determining appropriate
sample volume; an investigator must develop the ability to make such an
estimate. Erroneous estimates, however, may result from an abundance of
microscopic zooplankton. Accordingly, it is usually prudent to make a pre-
liminary shipboard microscopic examination of samples to determine the abun-
dance of the main biotic components. This may prevent the collection of
water samples that are biologically sparse, resulting in enumerations of
questionable statistical validity. Biologically sparse samples usually
contain insufficient numbers of the rarer species, and thereby produce
erroneous community evaluations.
6.2 Live Sample Analysis
Identification and enumeration of natural communities should be performed on
live material as the addition of preservatives renders many forms
12
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morphologically indistinguishable from detrital material. Rapid ship-board
analysis of aliquots for enumeration of fragile forms is recommended because
community alteration occurs quickly in confined containers. Sample aliquots
should be chilled to about 4°C and examined within twelve (12) hours. Pre-
screening with 333 micron netting to remove the larger filter feeding her-
bivores is advisable if aliquots are to be chilled and held.
6.3 Sample Fixation
After removal of the aliquots for live analysis and other ancillary tests,
the sample should be immediately treated with an appropriate preservative,
in order to stop all biological activity and fix the phytoplanktpn morphology
and cytology for later identification or examination. In practice, no
universal fixative has been developed. The selection of an appropriate
fixative to stabilize the desired cell characteristics often results in
preservation of two or more aliquots with different fixatives. For general
identification and enumeration, investigators commonly use neutral or
slightly basic formaldehyde (40%), neutralized with borax, sodium tetraborate
or sodium carbonate to pH 7.0 - 7.3. Various concentrations of formaldehyde
are used. If the samples are to be analyzed within a few days slightly lower
concentrations may be used. The appropriate concentration range is from two
to five milliliters of neutral formaldehyde per one hundred milliliters of
seawater. Concentrations of fixative in excess of five percent produce
progressive cellular distortion and shrinkage. Formaldehyde causes flagel-
lated forms to shed flagella and radically distorts or ruptures the naked
forms. It is generally used for diatoms, thecate dinoflagellates, and
cocolithophores. The addition of sucrose improves fixation of the cellular
fine structure.63 A few drops of saturated cupric sulfate solution per liter
of fixed sample retards the loss of chloroplast color and thereby aids in
distinguishing phytoplankton from detritus. Clumping of the settled material
frequently interferes with analysis. The addition of an emulsifying agent
helps in dispersal of clumps. Detergents, however, interfere with the
preparation of slides and should be used only when essential for clump
dispersion.
A second commonly used fixative, Lugol's solution (2 gm potassium iodide, 1
gm iodine in 200 ml distilled water), appears to be more effective at flagella
retention for many species. Enough Lugol's solution is added to sample to
yield a weak tea color. If the organisms are stained too darkly the color
intensity may be decreased with the addition of sodium thiosulfate. Lugol's
solution is not recommended for long term preservation because it slowly
decomposes; when the sample is faded the addition of fresh fixative is
required.
Many other fixatives have been developed for use with particular plant groups.
Some investigators fix two or more aliquots of the same sample with different
fixatives to take advantage of the special features of the various fixatives.
Chilling of the sample before and during fixation seems to give better re-
sults in preservation. The proper buffering of fixatives is of considerable
importance in preventing the cellular structural components from dissolving.
Some of the more specialized fixatives are Bouin's, Allen's (PFA), Schaudinn's
and von Rath's fixative. Those containing ethanol, acetic acid, or formic
13
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acid form precipitates when added to sea water and can be used only after a
sample has been concentrated. These fixatives are often very effective in
the preservation of various cytological features. ^""^
The preparation and fixation of phytoplankton for standard and scanning
election microscopy requires special care. The advantages of electron
microscopy in phytoplankton identification are unquestionable.67-69 The
initial microscope cost remains the major deterrent to its widespread use.
As more electron microscopes come into general use many long existing
taxonomic problems may be resolved. Osmium tetroxide and glutaraldehyde
are frequently used in cell fixation but present extreme exposure hazards
and require extra caution.
14
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SECTION 7
SAMPLE CONCENTRATION
There are three basic methods which are generally used for concentrating
samples: settling, centrifugation, and filtration. All procedures result
in the loss of cells, and the extent of loss is dependent on numerous factors.
Some of these are settling time, centrifugation time and speed, filter type
and mesh size, and cell morphology. The accuracy of enumeration is highly
dependent upon the researchers care and skill in sample manipulation. Gen-
erally, the fewer the manipulative steps the smaller the induced error.
7.1 Settling
Concentration of the preserved community by settling is often carried out in
the original storage containers. After allowing a minimum of forty eight
(48) undisturbed hours the supernatant can be carefully siphoned off. Si-
phoning should be slow, so as not to disturb the settled material.
An alternative procedure for handling of dense samples is to resuspend all
particulate material by vigorously shaking the sample and immediately pouring
a predetermined aliquot volume into a graduated cylinder. After settling,
the supernatant should be siphoned off with extreme caution. The final con-
centrate volume sample should include the liquid and cells from repeated
rinses of the concentrating cylinder.
7.2 Centrifugation
Modern methods of continuous flow centrifugation have eliminated many of the
early problems of cell loss. A number of problems, however, still exist.
The diversity of cell size, shape and flotation mechanism results in widely
differential settling times.70"'3 Some flagellates are highly resistant to
centrifugation, requiring speeds in excess of 18,000 rpm, while other more
fragile forms may lose flagella and other morphological appendages at con-
siderably slower speeds. Centrifugation is satisfactory for fluorescence
techniques. (See 8.4 Fluorescent Microscopy).
7.3 Filtration
The use of filtering techniques and methods including molecular filters has
advanced rapidly in recent years. Procedures use either vacuum or pressure
to facilitate the movement of the liquid portion of a sample through the
filter. Samples may be filtered singularly or in multiple sampling manifolds
filtering up to thirty simultaneous samples. Live organisms may be filtered
15
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and used for culture or productivity analysis. Preserved samples can be
concentrated on a gridded filter and mounted on microscope slides for iden-
tification and enumeration. A wide selection of filter materials and pore
sizes is available. Ancillary procedures requiring filtered samples include
liquid scintillation counting and binding assays for proteins, enzymes,
nucleic acids and other super-molecules.64,74-80
16
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SECTION 8
PHYTOPLANKTON ENUMERATION
The enumeration of phytoplankton is indispensable in community analysis.
Lund and Tailing propose three advantages in direct optical observation: 1)
evaluation of cellular variability, age, growth, shape and general physical
state, 2) estimation of relative abundance of both common and rare species,
and 3) determination of species present and their relative positions in the
community. I There are many methods for microscopic enumeration, each having
advantages and disadvantages. These methods employ a variety of techniques
including settling chambers for inverted microscopy, counting chambers for
standard microscopy, and membrane filters for both standard and scanning
electron microscopy. Ancillary automated methods for size and pigment quan-
tification are valuable for extended evaluation of community dynamics. The
evaluation of individual species is aided by the use of enrichment cultures.
61-82 Examples of these various methods and techniques are presented sep-
arately to aid the investigator in selecting the appropriate procedures for
his or her particular needs. The specific procedural details, advantages and
limitations can easily be found in the literature and should be scrutinized
to assure that the selected method will provide the desired quality of
enumeration.
8.1 Utermb'hl Method
Probably the best known and most widely accepted technique of phytoplankton
enumeration is the Utermohl method. According to this technique, a preserved
sample is placed in a vertical chamber and allowed to settle. The chamber
bottom is cover-slip thin and observation is made from beneath the chamber
using an inverted microscope. This sedimentation method permits the inves-
tigator great flexibility. Variable volume settling chambers permit adjust-
ments in aliquot size to ensure proper cell densities for accurate analysis.
The inverted microscope permits a full range of magnification, allowing
Kohler illumination, dark field, phase contrast, and oil immersion. When
necessary, cells may be manipulated or removed from the chamber for closer
examination. Disadvantages include the necessity of allowing sufficient time
for all cells to settle to the bottom of the chamber. This settling time is
a function of the column height and cellular morphology. Preconcentration of
samples permits the use of small volume chambers and shortens the settling
time. A second disadvantage results from the necessity of using preserved
samples. Many community surveys are limited to the preservable phytoplankton
because of the difficulties in accurate identification and enumeration of the
many naked flagellates.71,83-91
17
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8.2 Conventional Counting Method
The oldest method of phytoplankton enumeration that is still widely used
employs a shallow-chamber slide and conventional compound microscopy. The
most frequently used slides are the Sedgwick-Rafter, the Palmer-Maloney,
and the haemocytometer counting chambers. Advantages of these chambers
relate to their ease of use. Samples can be examined with a minimum of
preparation, and the chambers are appropriate for live or preserved samples,
permitting quick analysis of gross community characteristics. They also
reduce the problems of detrital interference and obstruction. The primary
disadvantage of the Sedwick-Rafter and the Palmer-Maloney chambers is that
only low magnifications can be used. This limits the enumerations to large
cells and often prevents positive identifications that are based on skeletal
fine structure details. A second problem results from the tendency of the
cells to form a nonrandom distribution within the chamber. If only a frac-
tion of the chamber is to be enumerated, procedures outlined by Jackson and
Williams should be used.92 The haemocytometer may be used for small cell
identification and enumeration but quickly becomes clogged if larger cells
are introduced. It has received considerable use in culture studies but is
not a practical chamber for natural community analysis. Lund developed aji
inexpensive nannoplankton counting chamber which can be used with intermediate
magnification. This chamber suffices for the identification of all but the
smallest phytoplankton.81*88'92"99*
8.3 Particle Counters
The use of an electronic particle counter for the assessment of a natural
phytoplankton community has met a considerable number of partially resolved
problems. The Coulter Counter records the changes in conductivity caused
by particles as they pass through a small sampling aperture. Phytoplankton
analysis methods have been adapted from the particle counter use in hema-
tologial analysis. Its application in algal culture analysis, where the
population cell sizes all fall within relatively narrow range, has been
generally accepted. In natural populations, however, problems of a very
wide range of cell size and shape have only begun to be resolved. Beryozkina
has proposed a theoretical classification of cells based on the morphometric
complexities of form, size, chromatophores, cell contour, and the number of
extreme points.1"** The adaptability of this classification to the capabil-
ities of the counter differentiation of these characters has yet to be demon-
strated. Additional problems are the overlap of cell sizes of large phyto-
plankters and small zooplankters and the presence of detrital material. "
8.4 Fluorescence Microscopy
Investigations involving the separation of the autotrophic and heterotrophic
communities often employ fluorescence microscopy techniques. Under proper
lighting conditions and with the addition of acridine orange dye the chloro-
phyll bearing parts of the cell will produce a bright red fluorescence while
the rest of the cellular material will fluoresce green. This differential
fluorescence enables separate counting of the photosynthetic and the hetero-
trophic communities. The microscopy technique allows analysis of freshly
collected samples containing live organisms or samples preserved with five
18
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percent (5%) glutaraldehyde. The technique requires a completely darkened
room because any background light obscures the fluorescence. Additionally,
chloroplasts of dead autotrophic organisms will fluoresce making live-cell
separation difficult. Finally, the Petroff-Hausser counting chamber has a
very small volume and is prone to clogging and cell distributional
anomalies.104-105
19
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SECTION 9
PRIMARY PRODUCTIVITY
The measurement of primary productivity by the 14^, light-dark bottle technique
is widely accepted as the only useful open ocean survey method. Oceanic sam-
pling usually necessitates measurements to be made from a vessel which is
either underway or on station for short time periods; the l^C method is well
suited for these conditions. It is also highly adaptable to a wide range of
experiments. These experimental uses fall into two general types: incubator
experiments and in situ experiments. Adaptations of the incubator usage
involve the choice between natural or artificial light. Variations of the
in situ method involve a choice of sample depths and incubation depths. All
methods include variations in incubation time. The in situ method is believed
to best reflect natural conditions but is not easily adaptable to routine
ocean surveys. The in situ method should be done concurrently with incubator
experiments whenever possible, to fulfill the continuing need for comparative
data. The recommended methodology by Ahlstrom and SCOR-UNESCO should be
adhered to when undertaking any primary productivity investigations. 06-119
20
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SECTION 10
PHYTOPIGMENT FLUORESCENCE
The investigation of phytoplankton productivity in the oceans has developed
along two separate lines. One is the estimation of primary productivity as
measured by photosynthetic rates. The most widely used method for this is the
C light-dark bottle technique described in section 9.0 primary productivity.
An alternate approach is the estimation of phytoplankton standing stock. In
addition to identification and enumeration procedures, the measurement of
pigment concentrations provides an estimate of the size of the phytoplankton
community. Concentrations of chlorophyll are measurable through their ability
to fluoresce. Fluorescence is the capacity of a pigment to absorb light at
one wavelength and to emit that energy at a lower wavelength. The intensity
of this fluorescence may be used to estimate the amount of chlorophyll, which
in turn may be used to estimate the phytoplankton standing stock. Many pro-
cedural variations have been developed for the extraction of chlorophyll from
the cells and for the measurement of fluorescence using filter fluorometers.
Measurements of fluorescence are highly sensitive, permitting the use of small
sample volumes and minimal light scattering interference. With the use of
selective filters chlorophyll a_ can be distinguished from detrital sources.
However, chlorophyll ai fluorescence emission ranges over a rather broad band
and overlaps with the fluorescence of other chlorophylls. ^5,106,114,120,125
A method of in vivo chlorophyll fluorescence measurment was developed by
Lorenzen. This method is approximately only one tenth (1/10) as sensitive
as extraction procedures, but its continuous-flow features present obvious
advantages. The in vivo measurements exhibit large inconsistencies which
partially arise from the community's general physiological condition, its
recent incident radiation history, and the variable ratios of chlorophylls
and ancillary pigments. This variability requires extreme caution in the
treatment of fluorescence data. A linear relationship between the in vivo
fluorescence and extracted fluorescence has been reported.106,114,127,126-
130
21
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SECTION 11
SOLAR RADIATION
The measurement of radiation is broken into two basic divisions; incident
solar radiation and solar radiation in the water column. Incident solar
radiation is the total sea level radiant energy of both the sun and the sky.
A broad spectrum radiant energy detector or pyranometer is equally sensitive
to the total wavelength span, including ultraviolet and infrared along with
the visible spectrum. Thus these measurements do not necessarily correlate
directly with biological activities below the sea surface. The spectral
distribution of the incident solar radiation has been determined and it is
possible to estimate the quanta and attenuation coefficients in specified
spectral regions. The radiant energy within a particular spectral region
at any particular depth can then be estimated. These data are then correlated
with other measurements of standing stock and primary productivity in attempt-
ing to qualify the exchange of radiant energy in the ocean.
The second aspect of solar radiation is that portion of energy available at
various depths below the sea surface. The problems associated with subsurface
radiant energy measurement are unresolved because of inherent difficulties in
distinguishing between available energy input and the energy that is utilized
in photosynthesis. There is a need for further studies involving correlations
between photosynthetic productivity determinations, absolute irradiance below
the surface and the relative incident radiation.106,108,114,131-133
22
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SECTION 12
ANCILLARY HYDROGRAPHY
All marine and estuarine surveys should include rather extensive hydrological
analysis. Most of the parameters regularly included in a hydrographic survey
are measurements of substances which effect organic production. In addition,
most of the procedures are adaptable to conditions encountered at sea while
maintaining a relatively high degree of accuracy. Generally, procedures are
available which require fairly simply apparatus and can be quickly mastered
by inexperienced technicians. Automated sample analyses have been developed
that, when budgetary conditions permit, improve efficiency.
Common relevant hydrographic measurements can include salinity, pH, carbon-
ates, inorganic micronutrients, dissolved oxygen, and dissolved organic
compounds. The specific procedures to be followed are thoroughly covered
in Strickland and Parsons' handbook.114,134
23
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SECTION 13
STATISTICAL CONSIDERATIONS
The estimation of a marine or estuarine phytoplankton community that is
inhabiting a particular body of water is subject to extensive extrapolations.
The identification and enumeration of phytoplankton involves the analysis of
a small fraction of an aliquot which was taken from a specific water parcel,
perhaps taken from a heterogeneous larger water mass. The need for using
appropriate statistical analysis is therefore clearly evident. Accordingly,
the development of a useful monitoring or baseline survey demands an adequate
awareness of the encountered statistical problems. These" problems fall into
three general groups. First, the development of the field sampling design
which will result in the accumulation of samples representative of the area
to be investigated. The problems of nonrandom distribution of organisms into
clumps or patches, which themselves may be randomly or non-randomly distri-
buted, was discussed in the sections on ecology and sampling design. Second,
the method of sample treatment and the method of sample analysis present
their own statistical pecularities. Each manipulation of a sample results
in an error factor. These errors are cumulative in nature and must be both
accounted for and held to a minimum. Third, there are a wide variety of
manipulative procedures that can be applied to the obtained sample values.
Multivariate factor analysis for marine systems is in the development stages
with a continual barrage of new literature on various models and theories.26.,
38,135-148 The phytoplankton community is commonly regarded from a variety
of perspectives including cell density, evenness, equitability, diversity.
ordination, recurrent group analysis, associations, and cluster analysis. °»
150-162 standard texts such as Boesch, Cochran, Deming, Fisher, Fryer,
Hirsch, Pielou and Siegel should be consulted for general theory and
methodology.35,36,143,162-166 xhe abundance of literature on population
analysis and the interrelationships of various parameters prohibit specific
reference. A close examination of the statistical bibliography will serve
as a convenient starting point for the novice statistician.
24
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SECTION 14
REFERENCES
Topical bibliographies are provided as a supplement to the referenced liter-
ature. Many of the bibliographic entries contain pertinent information on
multiple topics and their placement under a singular category was arbitrary.
Bibliographic entries are made under a single topic without cross-reference or
duplicate entry. The referenced material is included in the bibliographies.
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6. Steidinger, K. A., J. T. Davis and J. Williams. 1967. Dinoflagellate
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10. Graham, H. W. 1941. Plankton production in relation to character of
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37. Lassiter, R. R. and D. K. Kearns. 1974. Phytoplankton population
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TECHNICAL REPORT DATA
(Please read Instructions on the reverse before completing)
1. REPORT NO.
EPA-600/3-78-025
2.
3. RECIPIENT'S ACCESSION NO.
«. TITLE AND SUBTITLE
PHYTOPLANKTON SAMPLING IN QUANTITATIVE BASELINE AND
MONITORING PROGRAMS
5. REPORT DATE
February 1978
6. PERFORMING ORGANIZATION CODE
7. AUTHOR(S)
Paul E. Stofan and George C. Grant
8. PERFORMING ORGANIZATION REPORT NO.
Special Scientific Report
No. 85
3. PERFORMING ORGANIZATION NAME AND ADDRESS
Department of Planktology
Virginia Institute of Marine Science
Gloucester Point, VA 23062
10. PROGRAM ELEMENT NO.
1 BA 025
11. CONTRACT/GRANT NO.
EPA-R-804147010
12. SPONSORING AGENCY NAME AND ADDRESS
Corvallis Environmental Research Laboratory
Office of Research and Development
U.S. Environmental Protection Agency
Corvallis, Oregon 97330
13. TYPE OF REPORT AND PERIOD COVERED
Final Report
14. SPONSORING AGENCY CODE
EPA/600/02
15. SUPPLEMENTARY NOTES
16. ABSTRACT
An overview of phytoplankton sampling and analysis methods as they apply to
quantitative baseline and monitoring surveys is provided. A need for inclusion
of a preliminary field survey of the area under investigation and of flexibility
in sampling design is stressed. An extensive bibliography pertinent to phyto-
plankton sampling and analysis is included in the report.
This report was submitted in fulfillment of Contract No. R804147010 by the
Virginia Institute of Marine Science under the sponsorship of the U. S.
Environmental Protection Agency. This report covers a period from 24 Nov 75
to 31 May 77, and work was completed as of 15 Sept 77.
17.
KEY WORDS AND DOCUMENT ANALYSIS
DESCRIPTORS
b.IDENTIFIERS/OPEN ENDED TERMS C. COSATI Field/Group
Marine biology
Sampling
Water pollution
Phytoplankton
08/A
18. DISTRIBUTION STATEMENT
Release to Public
19. SECURITY CLASS (ThisReport)
unclassified
21. NO. OF PAGES
92
20. SECURITY CLASS (Thispage)
unclassified ,
22. PRICE
EPA Form 2220-1 (R«v. 4-77) PREVIOUS EDITION is OBSOLETE
84
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