See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/15359669

Marine Ecosystem Health Implications for Public

Health

Article  in  Annals of the New York Academy of Sciences · January 1995

DOI: 10.1111/j.1749-6632.1994.tb19850.x · Source: PubMed

CITATIONS READS
24 51

4 authors, including:

Timothy E Ford Cristina Possas

University of Massachusetts Lowell Fundação Oswaldo Cruz
208 PUBLICATIONS   6,392 CITATIONS    125 PUBLICATIONS   1,058 CITATIONS   

SEE PROFILE SEE PROFILE

Some of the authors of this publication are also working on these related projects:

Mother-to-Child Transmission of HIV View project

Environmental Health Equity View project

All content following this page was uploaded by Cristina Possas on 09 November 2021.

The user has requested enhancement of the downloaded file.

 Marine Ecosystem Health
Implications for Public Health
PAUL R. EPSTEIN
Haward Medual School
The Cambdge Hospital
1493 Ca&&e Street
Cambri&e, Massachusetts 02139
TIMOTHY E. FORD, CHARLES PUCCIA,
AND CRISTINA DE A. POSSAS
Haward School of Public Health
665 Huntington Avenue
Boston, Massachusetts 02115

AGENDA FOR THE WATERBORNE DISEASE DISCUSSION

A recurrent theme across disciplines of health, ecology, and medicine
suggests that alterations to the aquatic environment directly and indirectly
result in increases in waterborne disease outbreaks. A new research agenda
to address the effect of environmental change on human health must be
comprehensive and result in implementation plans for mitigation and preven-
tion. The ability to understand the connection between ecosystem structure
and function, and the epidemiology of disease can result in informed policy
decisions in such diverse areas as resource management, water and waste
treatment, agricultural and industrial practice, education, and in disease treat-
ment options.
There are at least four subtopics for this workshop:
1. We need to improve our understanding of the environmental factors
involved in the emergence, uncontrolled growth, persistence and transmission
of pathogens and pests.
2. While we cannot forecast an organism’s response to habitat alterations,
we can identify stressed ecosystems and critical regions where pathogedpest
emergence becomes more probable. We need to identify the potential risks
associated with specific environmental vulnerabilities and perturbations.
3. We need to develop surveillance to detect habitat changes and shifts
in bioclimatic conditions relevant to natural biota. Total surveillance, beyond
being impractical, may be unnecessary: Key species and elements may serve
as biological indicators of ecosystem stress and vulnerability. We need to set
goals for surveillance and explore the appropriate use of new technologies
while emphasizing simple, inexpensive, easily transferrable information sys-
tems and methodologies. And we need to integrate health surveillance with
13
14 ANNALS NEW YORK ACADEMY OP SCIENCES

other programs to monitor environmental and ecological health (diversity,

resilience, dynamic stability, productivity and vigor-see Epstein, this
volume).
4. Lastly, we need to discuss the nature of public health measures to
control, prevent, or ameliorate new and recurrent disease. Part of disease
recognition derives from the social implicationsof a disease and the perception
of risk. Interventions involve assessment of effectiveness and feasibility of
application, and of how best to surmount the social and economic barriers
that invariably present major obstacles to implementing successful public
health policies.
This introductory paper will briefly review OUT current understanding
of the interrelationships between the health of aquatic environments and
waterborne disease.

WATERBORNE DISEASES
Eighty percent of reported disease outbreaks are caused by waterborne
organisms (egocryptosporidiosis and cholera) or can be traced to a water-
borne source (eg., legionellosis). Environmental conditions, stresses and per-
turbations contribute directly to all these diseases. Between the 1960s and
1990, the average annual number of documented waterborne disease out-
breaks (WBDOs)in the United States increased almost fourfold. Giardia was
the most commonly identifiable WBDO, but improved techni ues implicate
91
Cyptospm'dium in an increasing number of episodes.' (Note e thousands
infected in Milwaukee in March, 1993.) In addition, the majority of cases of
acute gastroenteritis caused by waterborne organisms, although of unknown
etiology, are most likely of viral origin2Although many of the WBDOs in
developed countries can be traced to failure of treatment systems, or leakage
within distribution networks, an alarming number of outbreaks are caused
by resistance to commonly used concentrations of disinfectants. The obvious
example are the cysts that enable protozoa such as Giardia and Ctyptosporidia
to survive in treated water systems. In addition, algae in freshwater systems
absorb chlorine (forming hazardous chlorinated hydrocarbons) and reduce
effective free chlorine. Increasing evidence suggests that even in developed
countries there is a ublic health issue not addressed by current water quality
1
criteria, many of w ich themselves are rarely met.

Cholera
In marine systems, the story of cholera highlights how environmental
change (or anthropogenic influence) affects disease transmission. In the
1990s, following a decade of relative stability, cholera invaded the American
continent and resurged in Africa, and a new strain has now emerged in Asia.
This raises a variety of public health issues concerning food and water safety
(the "internal" environment of affected nations). However, the major focus
EPSTEIN et d.:MARINE ECOSYSTEM HEALTH 15

of this workshop is on environmental factors influencing the ‘cinoculum,yy

penetration, and persistence of organisms, including this ancient pathogen.
In 1961 cholera left Asia, arriving in southeastern Europe and Africa in
the 1970s, tracking coastlines and inland waterways. During the 1980s the
sum of cases worldwide declined but the number of affected nations grew
t h r e e f ~ l d In
. ~ 1991 cholera struck Peru, penetrating its poor populations
from multiple epicenters along the Atlantic The pandemic spread
rapidly to Ecuador (February), Colombia (March), and Chile (April), in
seaports up to 1700 km from the initial assault. Cholera later entered Brazil,
Venezuela, and Bolivia, again following rivers and streams. Over 15 months,
more than 0.5 million persons fell ill and close to 5,000 died in nineteen
Latin American nations;5 the toll in Africa was greater, with case-fatality
rates over 9%. From March to August, 1991, Vibrio cholerae 01, biotype El
Tor, serotype Inaba was isolated from marine plankton near Lima.6 V. cholerae
0 1 has been recovered from the bilge of Latin American vessels docked in
US Caribbean ports7 and it presumably crossed the Pacific as a stow-away,8
as DNA probing demonstrates “genetic identity” with the strain in Ban-
gladesh.
Since 1960 researchers in Bangladesh have related the seasonality of chol-
era to coastal algal blooms,lOJ1 but the reservoir remained a mystery. In
seeking to understand the survival strategy, Colwell and colleagues used
fluorescent antibody and polymerase chain reaction techniques, and identified
a viable but non-culturable, “quiescent,” form of V. cholerae (see Colwell and
Huq, this volume), associated with a wide range of surface marine life.12
Under adverse conditions, organisms contract 15- to 300-fold and reduce
their metabolic rates, in effect “hibernating,” in order to tolerate shifts in
pH, temperature, salinity, and nutrients. With favorable conditions (ea.,
sufficient nitrogen and phosphorus and proper water temperature) conducive
to algal blooms, Vzhio cholerae revert to a culturable and infectious state.
Chitina~es’~ and m~cinases’~facilitate attachment to aquatic organisms, while
algal-derived surface films and slimes enhance growth by creating turbulence-
free micro- environment^.'^ Prolonged survival of Vibriocholerae 01 and non-
0 1 strains is associated with cyanobacteria (Anabaena vaariabih), silicate
diatoms and drifting dinoflagellates, seaweeds and macroalgae (RrcopLyllum
nodosum), duckweed (Lemna minor) and water hyacinths (Eichhornia mas-
s@). Up to lo6bacteria have been detected on the egg sacs ofthe zooplankton
copepods. Near Lima, Vibrio cholerae 01 was isolated from mollusks, and
from the slun and intestines of fish.6
In Asia multiple-drug resistant strains of V . cholerae 01, biotype El Tor
are increasingly widespread. In 1992, chlorine-resistant forms of El Tor V .
cholerae were isolated in sewage lagoons near Lima, and several variants of
an entirely new strain, V. cholerae non-01 CT+ (non-agglutinating with
cholera enterotoxin) are now spreading in India, Bangladesh and Thailand.
Tendering a new antigen (0139) and bearing a pilus colonization factor, V .
cholerue non-01 CT+(0139 Bengal) appears to be exceptionally hardy in
terms of environmental adaptation (R. B. Sack, personal communication).
Extensive monsoon flooding in July 1993 enhanced its dissemination. The
16 ANNALS NEW YORK ACADEMY OF SCIENCES

genetic shifts in V. cholerae are especially disruptive as recombinant vaccine

trials for El Tor are beginning, and, with the potential of spread to immunolog-
ically naive populations in Africa and Latin America, 0139 Bengal could
become the agent of an eighth pandemic of cholera.

Marine Viruses
Massive North Sea seal kills (18,000) in 1988, and dolphin die-offs in
the western ( 1990) and eastern Mediterranean (1992) have been associated
with several strains of morbilli (phocinedistemper) viruses.l6 While pollutants
(eg.,PCBs) may increase sea mammal susceptibility to infection, it is now
clear that vast numbers of viruses exist in marine waters (see below). The
role of environmental changes in increasing the pathogenicity of marine
viruses, or creating conditions for the survival of known pathogenic viruses
may become a crucial question for the health of aquatic ecosystems.
Work of Paul and others,17 suggests that viruses are extremely abundant
in marine systems though we are uncertain of their role. However, there is
increasing evidence through improved enumeration techniques and electron
microsco y of high viral “infection” rates in bacteria-estimated to possibly
R
be as hig as 70 percent of heterotrophic bacteria-contributing to 10-100
percent of bacterial mortality.18 If this is the case, viruses may play a crucial
role in regulating productivity within the marine ecosystem, completely chang-
ing our understanding of trophic dynamics.
We are beginning to see strong correlations between drinking water and
gastrointestinal disease outbreaks,l9 suspected to be caused by viruses that
have survived treatment systems and that are substantially more abundant in
drinking water than previously suspected.20This is not limited to coastal
waters polluted by human sewage, where hepatitis A and Norwalk viruses
in shellfish often cause epidemics.21We should therefore not be surprised at
the magnitude of the potential roles for viruses in marine ecosystem health.
For example, at the November, 1993 meeting of the Environmental
Management of Enclosed Coastal Seas (EMEX) it was reported that the Long
Island brown tide, causing anoxic damage to scallops for several years, is now
producing a toxin, and a virus may be involved.

Advanas in Technology
Improvements in nucleic acid technology throughout the 1980s have
enabled us to characterize the community DNA of natural bacterial and viral
populations. Further purification of the DNA (or RNA) can enable molecular
probing for target gene sequences representing specific bacterial metabolic
potential.22Polymerase chain reaction technology (PCR) now enables detec-
tion of specific gene sequences from microorganisms that are present in
environmental sam les at very low concentrations. For example, PCR has
been used successdy to detect viable but non-culturableLegimtellapneumoph-
EPSTEIN et al.: MARINE ECOSYSTEM HEALTH 17

ila in water sam l e ~ In. ~addition,

~ PCR is now routinely used to detect
K
presence of the c okra toxin gene in V i h k cholerae samples.24
Our perception of the potential significance and risks of gene transfer in
the environment is dramatically changed by these new measurements of viral
and bacterial abundance. Anthropogenic activities may have created condi-
tions for increased gene transfer through discharge of heated, nutrient- and
pathogen-enriched waters. Although there are a number of mechanisms of
gene tran~fer,~’ the apparent abundance of viruses, and the high viral infection
rates of bacteria, suggest that transduction (whereby DNA is packaged into
viral capsids and subsequently transferred to a recipient bacterial cell) could
be a significant route for dissemination ofgenes coding for antibiotic resistance
and virulence factors. Genetic alteration by mutation has been shown to
increase under environmental and as with infection of higher organ-
isms, viral infection of bacteria may also increase under environmental stress.
What this could mean in terms of “newly created pathogens” is a hotly debated
topic. It would certainly seem that the potential for an eighth cholera pan-
demic discussed previously, could have been caused by the non-01 strain
of V . cholerae either obtaining the cholera toxin gene by mutation or gene
transfer.

HARMFUL ALGAL BLOOMS

Survival and proliferation of athogens in algal blooms are not the only
f
concern. Toxic phytoplankton b ooms are associated with paralyuc (PSP),
diarrheic (DSP), neurotoxic (NSP), and amnesic (ASP) shellfish poisoning
as well as with histamine (scromboid), and ciguatera (CFP) fish poisoning.
Phytoplanktonologists describe a global increase of red, green, golden, biolu-
minescent, and brown algal blooms in marine, estuarine, and inland waters,
from points as diverse as California, North Carolina, Guatemala, Iceland,
Japan, Thailand, and the Tasman Sea.”,27
Harmful algal blooms (HABs) affect tourism, aquaculture, and human
health. The following is a sample of reports: in 1973 and 1974 blooms of
brevetoxin-producing (NSP-related) Gymnodinium breve blanketed Florida
beaches; in 1976 saxitoxin-producing G. catenatum bloomed off the Spanish
coast causing hundreds of cases of mussel poisoning; Pyrodinium blooms
have spread from New Guinea (1972) to Brunei and Sabah (1976), to the
Philippines in 1983 and 1987 (1,127cases and 34 deaths), and to the Pacific
coast of Costa Rica and Guatemala (1987) (26 deaths). In 1988, immense
toxic green gelatinous blooms caused by Chrysochmulinapolyepskdevastated
200 salmon f m s in Norway and Sweden (an estimated $200 million loss)
[pollution from rivers of eastern Germany was blamed]; and during the 1980s,
DSP from dinoflagellates spread from Japan, North and South America to
previously uncontaminated areas of Ireland, Portugal, Italy, India, Thailandz8
(see Todd and Tester, this volume).
The new appearances of HABs coincide with El NGo years (see p. 19);
18 ANNALS NEW YORK ACADEMY OF SCIENCES

~ .HABs
is this “global e p i d e m i ~ ” ~of ~’ one of the first biological signals of
global change (T. Smayda, personal communication)?

ENVIRONh4ENTAL FACTORS
While sunlight, pH, upwelling currents, winds, and river runoff plumes
govern the recise location and timing of plankton blooms, the major anthro-
ltd
pogenic uences are as discussed below.

Pollution
Excess nutrients from sewage and fertilizer effluents are the primary cause
of marine eutrophication; eroding soil and acid rain (from fossil fuel and
forestry combustion) add additional nitrogen and phosphorus. Small fresh-
water bodies lack dissolved carbonates, thus increased atmospheric COz can
also ‘‘fertilize” algal growth on ponds and sewage lagoons. Toxins, such as
lipophilic organic compounds (PCBs, PAHs), heavy metals, and pesticides
bioaccumulate in the food chain, causing histopathological changes (eg, he-
patic tumors in fish), physiological, and genetic damage in marine organisms;
additionally they alter immune function, algal growth, and thus ecosystem
dynamics. Increased ultraviolet-B waves pose a similar threat to individuals,
populations and the community structure of species within ecosystems. Oil
slicks and solid plastics have had major impacts on marine mammals and
seabirds, altering predation pressures.

Over-Harvesting
The over-harvesting of fin and shellfish (beyond levels to sustain long-
term potential yields), reinforces algal growth by reducing algivorous grazing.
According to the UN, nine of the world’s seventeen major fisheries are in
serious decline, four are depleted, and the remainder “fully-” or “over-ex-
~ ~ the 1970s over-fishing in the Northeast U.S. Shelf system
p l ~ i t e d . ”During
re laced cod and haddock with benthic species (eg.,skates); but the system
go
re unded in the 1980s under international agreement to limit coastal fish-
ing30 The ability of a marine ecosystem to recover from one stress (its
resllience) depends on the stability of other ecosystem elements.

Habitat Loss
Wetlands bridge terrestrial and marine systems with grasses tolerant of
both. These coastal habitats have multiple functions: as “nature’s kidneys,”
they filter nitrogen and phosphorus, store carbon, remove toxins, and support
fish and seabird communities. Salt marshes are suffering from coastal develop-
ment; each year the United States loses 300,000 acres of wetlands. Mangroves
EPSTEIN ct uf.: MARINE ECOSYSTEM HEALTH 19

are removed for mariculture. Coral reefs (the “oceans’ rainforests”), which
cradle diverse marine flora and fauna and buffer coasts from storms, are being
widely mined to supply material for road and housing construction in poor
nations.29In addition, warming and other stresses unsettle the algal symbiont,
bleaching coral by expelling swarms of dinoflagellate^;^^ additionally, algal
mats block light and deoxygenate the shoals. Most of the east African and
Indian reefs are severely disfigured, while marine reserves have begun to
protect some of the Caribbean and Pacific reefs.29

Warming and Algal Growth

Ship recordings (“sea truth”) since 1850 demonstrate ocean as well as
terrestrial warming.32Warming reduces dissolved oxygen, and, within ranges,
stimulates algal photosynthesis and metabolism. Warming also favors cyano-
bacteria and dinoflagellates, many toxic to rival species and less palatable to
zooplankton and fish grazers (a positive feedback on algal growth). During
the 1980s, the warmest decade of the century, several large-scale natural
experiments occurred. In 1982/83 a strong El Niiio (the strongest known
climate signal, with the broadest, reproducible impacts on regional weather
patterns throughout the world) warmed North Atlantic seas, altering zoo-
plankton, finfish, seal, and seabird communities throughout the decade. In
the Pacific, elevated sea surface temperatures overwhelmed cool upwelling
water, altering Peruvian sardine and anchovy yields for years.33 In 1987 (an
El Niiio year) there was extensive coral bleaching in the Caribbean and large
die-offs of sea-grass in the Florida Keys. In 1987 the first recorded G. breve
red tide was observed off Cape Hatteras, North Carolina. The Gulf Stream,
in which G. breve were always present at low levels ( < l o cells/l), robably
F
transported this phytoplankton. Blooms were apparently fostered by avorable
environmental conditions, including the presence of a semi-stable gulfstream
eddy serving as a “chemostat” for G. breve34 (see Tester, this volume).
Further up the Atlantic coast in 1987 a new phenomenon occurred.
Following heavy rains subsequent to drought (increasing runoff),and accom-
panying warm eddies of the gulf stream which swept unusually close to
Canada’s Prince Edward Island, the pennate diatom (Nitwchza pungem)
bloomed. The diatom produced domoic acid causing 156 cases of amnesia
(some permanent) and five deaths in Canadian mussel consumers35(seeTodd,
this volume). During the same period, hundreds of dead bottlenose dolphins
and humpback whales appeared on Northeast coasts, with PCBs, biotoxins
~ ~ 1987, outbreaks of domoic acid poi-
and “viruses” i m ~ l i c a t e d .Since
soning have spread: in 1991192 (also an El Nifio year), in Monterey Bay,
California (now a marine reserve),hundreds of pelicans and cormorants were
poisoned from ingestion of fish contaminated with domoic acid; then, in the
summer of 1992, massive blooms of a close relative, Pseudonztzrchiapsezrdodeli-
catkzma, occurred in Scandinavian waters.37 199111992 also saw the
first appearance of PSP saxitoxins as far south as the Straits of Magellan,38
concurrent with the penetration of V. cholerae into the Americas.
20 ANNALS NEW YORK ACADEMY OF SCIENCES

LARGE MARINE ECOSYSTEMS

Just as the major pandemics cross regional, national and international
boundaries, the underlying ecosystemfunctionsthat permit biologicalcommu-
nities to exist and persist depend on energy and material flow plus organismic
migrations across large regions. Some 49 large marine ecosystems (LMEs)
have been identified,33 with each area representing at least 200,000
km2. Global temperature changes, alterations in hydrography, and massive
human interventions such as overfishing, pollution or diversion of major
watershed areas disrupt LMEs, as dominant species migrate away, become
restricted, or are forced to change behavior patterns (see Sherman, this
volume).

Remote Sensin8 a d A&& Blooms

Remote sensing provides a potentially important tool for monitoring the
health of LMEs. The global distribution of coastal blooms can be visualized
on images from the Coastal Zone Color Scanner (CZCS), a satellite that
collected data from 1978 to 1985. Detecting visible red and near infrared
emissions, CZCS images provided estimates of the amount of chlorophyll 3,
thus generatingvalues for primary production and the biomass of phytoplank-
ton (see FIGS. 2-5 in Remote Sensing section). These values are used to
evaluate the role of marine life in the global carbon cycle. As algae are a
reservoir for enteric pathogens and a source of toxins, such images can also
be used for public health purposes. The Advanced Very High Resolution
Radiometer (AVHRR), detecting far infrared (heat), on satellites of the
National Oceanic and Atmospheric Administration (NOAA), is now used
to monitor phytoplanktonblooms (see FIGS.6-9 in Remote Sensing section).

a
AVHRR enerates images revealing river plumes, ofien associated with
blooms, w ich can indicate where sampling should be done for monitoring
toxic species (D. Anderson, WHOI, personal communication). The next
generation of satellites, Sea-ViewingWide Field Sensor (Sea-WiFS),is sched-
uled for launching in 1994.

CONCLUSIONS
The ublic health crises of new and resurgent diseases can in large part
cp
be trace to a failure in understanding the interactions between the human
population and the environment. Anthropogenic influence on the marine
environment, for example, enables development of conditions for pathogen
survival through eutrophication and heated waters. Genetic transfer can also
be afFected/accelerated by these conditions, resulting in enhanced develop-
ment of antibiotic resistance, exposure to virulence factors and to environmen-
tal stresses that help to select for virulence. Public health may be affected
indirectly throu h the food chain; we are only beginning to understand that
9
community he th is closely tied to the health of the ecosystem.
EPSTEIN ct ul.: MARINE ECOSYSTEM HEALTH 21

Several research questions follow, moving from the specific to the

more general.
1.How extensive are viable but non-culturable stages of human pathogens
(refuge strategies) and can we identify the environmental factors that result
in the return to virulent (and transmissible) states?
2. Can we quantify risks of genetic transfer/mutation within a specific
polluted aquatic environment?
3. How do we prioritize ecolo ical questions in order to model and assess
2
degrees of risk, and respond to e potential as well as actual outbreaks of
waterborne disease?
4. How might harsh environments and changes in predator/prey dynam-
ics, competitors and insurance species, contribute to the emergence, resur-
gence and/or redistribution of pathogens and pests?
5 . Can we measure the direct and indirect cascading effects of localized
pollution events at the large marine ecosystem or even global level?
6. How do global signals and changes within LMEs integrate to create
new habitats that permit the proliferation of new disease?
7 . How can environmental monitoring be enhanced to include indicators
of potential disease (eg.,algal toxins and bacterial symbionts) and the surveil-
lance of health outcomes?
8. How will environmentalmanagement to improve ecosystemhealth effect
disease emergence and resurgence?
Our advances in detection technology raise the question as to how exten-
sively our surveillance of environmental samples for patho ens or toxins
B
should become? In theory the applications and numbers o pathogens or
potentials to become pathogens are vast. Resources are, however, limited
and must be directed towards the major health crises that currently exist (eg.,
cholera) and the most informed estimates of where, and what emerging
epidemics might occur. Of immediate concern is 0 1 3 9 Bengal. Develo ment
E
of an early warning system for 0 1 3 9 Bengal, monitoring plankton and allast
water for vibrios (speciated) could constitute this system. This will involve
monitoring the basic parameters of LMEs with the participation ofthe Interna-
tional Maritime Organization, the WHO and CDC. An interdisciplinary
approach is required to begin to understand and close the gaps between
environmental and human health.

REFERENCES
1. ROSE,J. B., GERBA,C. P. & W. JAKUBOWSKI. 1991. Survey of potable water supplies
for Ctptarporirlium and Giurdiu. Environ. Sci. Technol. 25: 1393- 1400.
2. GERBA,C. P. & J. B. ROSE, 1990. Viruses in source and drinking water. In Drinking
Water Microbiology. G . A. McFeters, Ed.: 380-396. New York: Springer.
3. WHO, 13 March 1991. Cholera: The epidemic in Peru-Part I. Weekly Epidemiological
Record No.9. 66: 61-63.
4. WHO, 17 May 1991. Cholera in Peru-Update. Weekly Epidemiological Record No.
20. 66: 141-145.
22 ANNALS NEW YORK ACADEMY OF SCIENCES

5. SWERDLOW, D. L., E. D. MINTZ,M. RODRIQUEZ, et d.1992. Waterborne transmission

ofepidemiccholera in Trujillo, Peru: Lessons for a continent at risk. Lancet 340: 28-33.
6. TAMPLIN, N. L. & C. C. PARODI.1991. Environmental spread of Vibrio cbohue in Peru.
Lancet 338: 1216-1217.
7. DEPAOLA, A., G. M. CAPERS, M. L. MOTES,et d. 1992. Isolation of Latin American
epidemic strain of V W cbolerae 0 1 from US Gulf Coast. Lancet 339: 624.
8. CARLTON, J. T. & J. B. GELLER.1993. Ecological roulette: The global transport of
nonindigenous marine organisms. Science 261: 78-82.
9. FARUQUE, S. M. & J. ALBERT.1992. Genetic relation between Vibrio cbokerae 0 1 strains
in Ecuador and Bangladesh. Lancet 339: 740-741.
10. COCKBURN, T. A. & J. G. CASSANOS. 1960. Epidemiology of epidemic cholera. Public
Health Reports 75: 791.
11. SAMADI,A. R., N. K. CHOWDHURY, M. I. HUQ& M. U. KHAN. 1983. Seasonality
of classical and El Tor cholera in Dhaka, Bangladesh: 17 year trends. Trans. R. SOC.
Trop. Med. Hyg. 77: 853.
12. BYRD, J. J., X. U. HUAI-SHU& R. R. COLWELL. 1991. Viable but non-culturable
bacteria in drinking water. Appl. Environ. Microbiol. 57: 875-878.
13. NALIN,D. R., V. DAYA,A. REID, M. M. LEVINE& L. CISNAROS.1979. Adsorption
and growth of Vibrio cbokrae on chitin. Infect. Immun. 25: 768-770.
14. SCHNEIDER, D. R. & C. D. PARKER.1982. Purification and characterization of the
mucinase of V W cbohae. J. Infect. Dis. 145: 474-482.
15. JENKINSON, I. 1992. New-A seawater rheology group. H d Algae News. Suppl
to International Marine Science (UNESCO) 62: 5.
16. HEIDE-JORGENSEN, M.-P., T. HARKONEN, R. DIETZ& P.M. THOMPSON. 1992. Retro-
spective of the 1988 European seal e p k t i c . Dis. Aquat. Org. 13: 37-62.
17. PAUL,J. H. 1993.The advances and limitations ofmethodology.In Aquatic Microbiology:
An Ecological Approach. T. E. Ford, Ed.: 483-511. Boston: Blackwell.
18. PROCTOR, L. M. & J. A. FUHRMAN.1990. Viral mortality of marine bacteria and
cyanobacteria. Nature 343: 60-62.
19. PAYMENT,P., L. RICHARDSON, J. SIEMIATYCKI, R. DEWAR,M. EDWARDES & E.
FRANCO.1991. A randomized trial to evaluate the risk of gastrointestinal disease due
to consumption of drinking water meeting current microbiological standards. Am. J.
Pub. Health 81: 703-708.
20. BITTON, G., S. R. FARRAH,C. L. MONTACUE & E. W. AKIN.1986. Viruses in drinking
water. Environ. Sci. Technol. 20: 216-222.
21. EASTAUGH, J. 1989. Infectious and toxic syndromes from fish and shellfish consumption.
Arch. Intern. Med. 149: 1735-1740.
22. WEN, T. C. & L. JIMENEZ. 1988. Enumeration and identification of bacteria from
environmental samples using nucleic acid probes. Microbiol. Sci. 5: 340-343.
23. BEJ, A. K., M. H. ~ ‘ J B A N I& R. M. ATLAS. 1991. Detection of viable legionella
pneumophila in water by polymerase chain reaction and gene probe methods. Appl.
Environ. Microbiol. 57: 597-600.
24. SHIRAI,H., M. NISHIBUCHI, T. RAMAMURTHY, tt d.1991. Polymerase chain reaction
for detection of cholera enterotoxin operon of V W cbohae. J. Clin. Microbiol. 29:
1517-2521.
25. MILLER,R. V. 1993. Genetic stability of genetically engineered microorganisms in the
aquatic environment. In Aquatic Microbiology: An Ecological Approach. T. E. Ford,
Ed.: 483-511. Boston: Blackwell.
26. SMAYDA,T. J. & Y. SHIMIZU.1993. Toxic Phytoplankton Blooms in the Sea. UK:
Elsevier.
27. ANDERSON, D. M. 1992.The fifth international conference on toxic marine phytoplankton:
A personal perspective. Harmful Algae News, Suppl. to International Marine Science
(UNESCO) 62: 6-7.
28. LASSUS,P. 1993. Prospectus: Sixth InternationalConference on Toxic Marine phytoplank-
ton. Nantes (Xdex 01, France. (Contains multiple citations.)
29. SIMONS,M. 6 Aug 1993. Mining is ravaging the Indian Ocean’s coral reefs. New York
Times, p. 3.
EPSTEIN ct al.: MARINE ECOSYSTEM HEALTH 23

30. VALIELA, I. 1984. Marine Ecological Processes. New York: Springer-Verlag.

31. HAYES,L. & T. J. GOREAU.1991. The tropical coral reef ecosystem as a harbinger of
global warming. World Resource Rev. 3: 306-322.
32. HOUGHTON,J. T., G. L. JENKINS& J. J. EPHRAUMIS, Eds. 1990. Climate Change:
The IPCC Scientific Assessment. New York: Cambridge University Press.
33. SHERMAN, L., L. M. ALEXANDER& B. D. GOLD,Eds. 1993. Large Marine Ecosystems:
Stress, Mitigation, and Sustainability.: 301-319. AAAS Press.
34. TESTER,P. A,, R. P. STUMPF,F. M. VUKOVICH,P. K. FOWLER& J. T. TURNER.
1991. An expatriate red tide bloom, transport, distribution, and persistence. Limnol.
Oceanogr. 36(5):1053-1061.
35. TODD,E. C. D. 1993. Domoic acid and amnesic shellfish poisoning-a review. J. Food
Protection 56: 69-83.
36. MACKENZIE, D. 1988. Mystery of mussel poisoning deepens in Canada as the chain of
death spreads to whales. New Scientist 30 (28 Jan.).
37. LUDLOHM,N. & J. SKOV.1993. P r e u ~ n i ~ c b ~ p r e uin ~Scandinavian
~ l ~ ~ r waters.
i ~
Harmful Algae News. Suppl to International Marine Science (UNESCO) 62: 4.
38. CARRETO, J. I. & H. R. BENEVIDES. 1993. World record of PSP in southern Argentina.
Harmful Algae News. Suppl to International Marine Science (UNESCO) 62: 7.

View publication stats