EPA/230/R-92/011
December 1992
BIOLOGICAL POPULATIONS AS INDICATORS
OF ENVIRONMENTAL CHANGE
Office of Policy, Planning and Evaluation
U.S. Environmental Protection Agency
Washington, DC 20460
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This report, "Biological Populations as Indicators of Environmental Change - Volume I" is a review
of scientific literature on biological phenomena frequently noted in the popular press, to determine
the degree to which scientists are reporting that the phenomena may be indicators of environmental
changes.
Noticing that reports of events, such as dwindling numbers of warblers in our forests and apparent
reductions of frogs and salamanders observed worldwide, were appearing almost weekly in news
features and science pages of major newspapers, the Environmental Results Branch (ERB) of the
Office of Policy, Planning and Evaluation (OPPE), U.S. Environmental Protection Agency (USEPA)
began an attempt to identify existing knowledge about these phenomena. Of particular interest was
considering whether these phenomena, alone or in combination, might be indicators of environmental
change at the regional, continental, hemispheric, or global scales.
The first volume reviews eight of these phenomena; planned future volumes will address additional
occurrences and continue to monitor the literature on the topics in this volume. Selection of these
eight topics is not an indication that we believe these to be the "best" indicators of environmental
change; simply these appeared frequently in the popular press and data was more plentiful than for
other topics. Likewise neither do we suggest that one can determine if these changes are from natural
causes or are anthropogenic (induced by man). This is a scientific literature review "directed" by a
screen of articles appearing in the popular press; we make no independent recommendations nor
conclusions in regard to causes or selection of indicators of environmental change.
As part of this reference/educational document, extensive bibliographies are included. These
bibliographies, the scientific references cited in the text and included within each chapter as
"References", and popular literature cited as a "Popular Press Bibliography", should serve as tools for
scientists and the general public alike.
Questions or comments should be directed to Otto Gutenson, (202) 260-4909. If you would like
additional copies of this document please write:
Public Information Center MS3404
U.S. Environmental Protection Agency
401 M Street S.W.
Washington, D.C. 20460
or
The National Center for Environmental
Publications and Information
11029 Kenwood Road
Cinncinnati, Ohio 45242
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TABLE OF CONTENTS
Page
FORWARD v
EXECUTIVE SUMMARY . . . .". vii
ACKNOWLEDGMENTS xi
1. OVERVIEW OF BIOLOGICAL POPULATIONS AS INDICATORS OF
ENVIRONMENTAL CHANGE . 1
1.1. Selection of Indicators: Technical and Popular Literature Scan ...... 1
1.2. Methods , 3
1.3. References 5
2. SYNOPSIS OF EIGHT POTENTIAL BIOLOGICAL POPULATION
INDICATORS , . .... . 6
2.1. Neotropical Migrant Bird Species 6
2.2. North American Freshwater Fish 27
2.3. Ducks in North America . 41
2.4. Coral Reefs Worldwide 55
2.5. Amphibians Worldwide 73
2.6. Turtles Worldwide ............. 91
2.7. Marine Mammals 1.04
2.8. Forests Worldwide 120
3. CONCLUSIONS . 137
3.1. Summary of Relative Sensitivity of Ecological Indicators 138
3.2. Summary of Human Activities Causing Species Declines 140
3.3. Monitoring Environmental Change 145
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LIST OF EXHIBITS
Exhibit 1.
Exhibit 2.1.1.
Exhibit 2.1.2.
Exhibit 2.1.3.
Page
Biological populations as potential indicators of environmental
change 4
Migratory pathways of neotropical songbirds 8
Recent decline of neotropical migrant songbird populations .... 9
Decline in the number of winter resident warblers captured at the
Guanica Forest, Puerto Rico, between 1973 and 1988 112
Exhibit 2.1.4.
Exhibit 2.1.5.
Exhibit 2.1.6.
Exhibit 2.1.7.
Exhibit 2.2.1.
Exhibit 2.2.2.
Exhibit 2.2.3.
Exhibit 2.2.4.
Exhibit 2.2.5.
Exhibit 2.2.6.
Increase in percentage of nests preyed upon with decreasing forest
fragment size 13
Decreased incidence of cowbird parasitism with increasing distance
from forest openings 14
Increase in cowbird abundance in the United States since 1900 16
Proportion of woodlands of each size class in which the species
indicated were found in the District of Columbia or Maryland . 18
Numbers of taxa of native freshwater fishes of selected river
systems 28
Cumulative number of fish extinctions by decade in the United
States during the past century 29
Map of recently extinct fishes of the United States 30
AFS/ESC list of freshwater fish taxa in North America that are
endangered, threatened, or of special concern 32
Number of fish species endangered, threatened, or of special
concern by state 33
Proportion of freshwater fish species per 1,000 river miles
classified by AFS as endangered, threatened, or of special
concern by state 34
11
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Page
Exhibit 2.2.7.
Exhibit 2.3.1
Exhibit 2.3.2.
Exhibit 2.3.3.
Exhibit 2.3.4.
Exhibit 2.3.5.
Exhibit 2.4.1.
Exhibit 2.4.2.
Exhibit 2.4.3.
Exhibit 2.4.4.
Exhibit 2.4.5.
Exhibit 2.4.6.
Exhibit 2.5.1.
Exhibit 2.5.2.
Causes of extinctions and population declines in North
American freshwater fish
35
Changes in breeding population estimates for 18 duck species
included in US FWS census . 42
Changes in breeding population estimates for ten species of
ducks in 1991 compared with 1955 to 1990 43
US FWS mallard, northern pintail, and green-winged teal
population estimates for 1955-1991 45
Summary of the number of May ponds (adjusted for visibility)
in portions of Prairie Canada and the northcentral United
States, 1990 and 1991 46
US FWS May Breeding Waterfowl Survey estimates for mallards
from 1955 to 1991 using old and new estimation methods .... 50
Location of coral reef bleaching sites reported during
1979 to 1980 59
Location of coral reef bleaching sites reported during
1982 to 1983
60
Location of coral reef bleaching sites reported during
1986 to 1987 61
Location of coral reef bleaching sites reported during
1989 to 1990 62
Coral species richness and percent cover as a function of
sedimentation rate (mg/cm -day) in Guam 64
Model of causes of worldwide coral reef bleaching 67
Examples of declining amphibian populations in North America 75
Examples of declining amphibian populations in other areas . . 76
in
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Exhibit 2.5.3.
Exhibit 2.5.4.
Exhibit 2.6.1.
Exhibit 2.6.2.
Exhibit 2.7.1.
Exhibit 2.7.2.
Exhibit 2.8.1.
Exhibit 2.8.2.
Exhibit 3.
Page
Effect of logging on amphibian species number and density in
western Oregon , 79
Acid tolerance of natterjack toad development 81
Examples from the 107 species, or approximately one third of
the world's total number of land and freshwater turtle species,
that the World Conservation Union reported as threatened,
in danger of extinction, or heavily exploited 93
Sea turtle population trends 95
Mass mortalities of pinnipeds 108
Declining populations of pinnipeds 109
Percent of original forest cover remaining in the United States
and Middle America since 1500 122
Comparison of symptoms and possible causes of forest declines
in central Europe and eastern North America 126
Matrix of human activities and stressors that are or
may be impacting the eight groups of organisms reviewed
in this report 141
IV
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FORWARD
Global warming, acid rain, water pollution — how can the general public
understand which issues are the most serious and which ones, if any, are overstated?
What do we really know about the effects of these and other environmental problems on
the health of ecosystems and plant and animal populations within ecosystems? What do
news reports of unexplained (and sometimes previously unseen) occurrences such as
large numbers of dead dolphins washing up on the Atlantic coast of the United States
and in the Mediterranean, apparent reductions of frogs and salamanders observed
worldwide, and dwindling numbers of warblers in our forests really mean? Are these
occurrences.induced by man, i.e., are they "anthropogenic?"
After noticing that such events and related phenomena began to be identified
frequently in scientific journals and almost weekly in news features and the science pages
of The New York Times and The Washington Post, the Environmental Results Branch
(ERB) of the Office of Policy, Planning and Evaluation (OPPE), US Environmental
Protection Agency (US EPA), began an attempt to identify existing knowledge about
these phenomena. Of particular interest was considering whether these phenomena,'
alone or in combination, might be indicators of environmental change at the regional,
continental, hemispheric, or global scales.
This first volume examines certain of these phenomena and attempts to distinguish
those occurrences in the natural world that scientists believe to be anthropogenic from
those phenomena for which so little is known that *it is unclear whether these events
result from man-made or natural causes. Following volumes will consider additional
natural-world occurrences as potential indicators of environmental quality and will
continue to monitor the literature on the topics in this volume.
The scientific literature and popular information sources were reviewed
simultaneously, to determine the degree to which scientists are reporting that the
phenomena may be indicators of environmental changes, and to develop some indication
of public awareness and concern for these events. These bibliographies — the scientific
references cited in the text are included within each chapter as "References" and a
selected popular literature bibliography as "Popular Press Bibliography" - should serve as
tools for scientists and the general public alike. The use of popular information sources
as part of the screening process to identify biological phenomena of potential concern
was a different approach than typically is used in developing a scientific literature review.
However, such a "media scan" appears to be an appropriate tool to use on occasion.
This is in keeping with the new emphasis at all levels of government of collecting the
types of information that may be of particular interest to our "customers", the public.
Such media scans are one type of tool to help us take into account what may be of
special concern to the public in developing reference documents such as this.
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Twelve potential biological indicators of environmental change of particular
interest were identified in the initial literature review based on scientific merit and
validity. The US EPA is addressing two of these topics elsewhere. This volume focuses
on eight of the remaining initial topic areas. These eight topic areas were chosen
because of their broad geographic extents. Additional topics may be addressed in future
publications. Scientists with expertise in specific topics assisted in reviewing this
document for technical accuracy are listed in the acknowledgements section.
D. Eric Hyatt and Otto Gutenson, Editors
EPA Office of Policy, Planning and Evaluation
VI
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EXECUTIVE SUMMARY
We live in an era of unprecedented loss of biological diversity, and possibly of
certain life-supporting services provided by ecosystems. Recently, news reports of
occurrences such as large numbers of dead dolphins washing up on the Atlantic coast of
the United States and in the Mediterranean, apparent reductions of amphibian
populations - such as frogs and salamanders - observed worldwide, and dwindling
numbers of warblers in our forests, have been appearing with increasing frequency. But
what do these observations really mean? Which are natural occurrences in response to^
variability in weather or other natural phenomena, and which are consequences of man's
activities? What do these phenomena tell us about the condition of our environment?
Which of man's activities are the most damaging to our biological heritage, and what, if
anything can we do to reverse these losses?
The Environmental Results Branch (ERB) of the Office of Policy, Planning and
Evaluation (OPPE), US Environmental Protection Agency (US EPA) is beginning an
attempt to identify existing knowledge about these phenomena. Of particular interest is
considering whether these phenomena, alone or in combination, might be indicators of
environmental change at regional, continental, hemispheric, or global scales. To
accomplish this, an analysis of the scientific literature and popular information sources
was performed to determine the existing "state of the science" for such reported
phenomena. Twelve potential indicators of environmental change of particular interest
were identified in the initial review of news media and scientific journals (see page 4).
US EPA is addressing two of these elsewhere (loss of wetlands and loss of biodiversity).
This report focuses on eight of the remaining ten topic areas:
(1) Declining populations of neotropical migrant birds;
(2) Declining populations and increasing numbers of extinctions of North
American fish species;
(3) Decreasing populations of North American ducks;
(4) Increased incidence of coral bleaching, degradation, and death worldwide;
(5) Declining populations of amphibians worldwide;
(6) Decreasing populations of turtles worldwide;
(7) Mass deaths of dolphins and declining populations of seals;
(8) Loss of forests worldwide and forest "dieback" in the north temperate
zones.
VII
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Observed trends, hypotheses, and supporting evidence on causes of the trends for each
topic are described in Section 2 of this report and summarized briefly below.
Neotropical migrant bird species. Fragmentation of North American forests is
contributing to the decline of neotropical migrant bird species that breed in forest
interiors. Forest fragmentation exposes larger proportions of the remaining forest to
edge conditions and edge predators and parasites, and several characteristics of
neotropical migrant species make them more vulnerable to these changes than short-
distance migrants or resident species. The relative contribution of "island effects" of
forest fragmentation to the decline of neotropical migrants on a regional scale has not
been analyzed.
Tropical deforestation also might be contributing to the observed population
declines of neotropical migrant species, but scientists do not agree on this issue.
Whether or not tropical deforestation currently is contributing to the declining
neotropical migrant bird populations, it is likely to become a more serious problem than
fragmentation of habitat in North America in the near future. Obviously, continuing
tropical deforestation and North American forest fragmentation are likely to cause
continued population losses and eventual extinctions of neotropical migrant species.
North American freshwater fish. The rate of extinctions of North American
freshwater fish has risen sharply in the last decade. Now, fully a third of the native
species of North American freshwater fish are considered threatened, endangered, or of
special concern. Physical alteration of surface waters (e.g., channelization, dams,
reservoirs) and the introduction of non-native species are the major causes of population
declines and extinctions among North American fish, although- other factors have
contributed to the decline of many species.
Ducks in North America. Several species of ducks have suffered significant declines
in population levels in North America in recent years (i.e., mallard, American widgeon,
blue-winged teal, northern pintail, and redhead), and several other species appear to be
declining also (e.g., canvasback, northern shoveler, green-winged teal). Investigators
believe that the declines are due primarily to drought and human activities that have
severely reduced the abundance of wetland habitats required by ducks and other
waterfowl for breeding, migration, and overwintering. Crowding of birds into the
remaining areas may contribute to outbreaks of disease and increased mortality.
Degradation of the remaining wetlands by acid rain and/or agricultural runoff may be
reducing the reproductive success of ducks in the remaining habitats. Finally, uncovered
oil pits contributed to the mortality of migratory waterfowl, but regulatory actions over
the past few years have eliminated this source of mortality. Uncovered cyanide pits in
the mid-west, however, continue to pose a threat.
Coral reef communities worldwide. For years, coral reef communities have been
suffering from adverse effects of human activities, including physical destruction (e.g.,
Vlll
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boat anchors, coral mining), nutrient runoff and sedimentation, and coastal pollution,
from agriculture, industries, and sewage. In addition, during the 1980's, four coral reef
community bleaching events occurred on an unprecedented geographic scale. Scientists
believe that these wide-spread bleaching events occurred in response ,to elevated water
temperatures, but as yet there is no conclusive evidence that the bleaching events are
indicative of a global warming trend. John Ogden, director of the Florida Institute of
Oceanography, has concluded that "virtually every reef system in the world is suffering."
Amphibians worldwide. Recently, numerous reports of declining populations and
extinctions of amphibian species worldwide have raised the question of whether a
worldwide decline is occurring that may be a result of human activities. Although it is
not yet clear whether a true global decline is in progress, concern for that possibility
continues to increase. Habitat destruction, introduced species, habitat acidification, and
unusual climatic variations are known to have had adverse effects on several localized
amphibian populations. Other potential factors, such as pathogens, pesticide exposure,
and increased ultraviolet radiation, have not yet been studied. The cause(s) of many of
the observed declines of frog populations have not yet been identified, and additional
study is needed, particularly on the range of fluctuations that might be expected to occur
naturally.
Turtles worldwide. Approximately one third of the world's species of land turtles
(terrestrial and freshwater semi-aquatic) are now considered to require conservation
attention. Essentially all of the world's sea turtle species are considered threatened or
endangered. For the land turtles, habitat destruction and fragmentation, appear to be
the primary causes. Juvenile and adult sea turtles suffer primarily from capture by
shrimp trawlers, but other factors also cause excess mortality. Various human activities
have restricted available nesting beaches and have reduced the survivorship of sea turtle
eggs and hatchlings on remaining beaches.
Marine mammals. Two recent bottlenose dolphin mass mortalities have triggered
public and scientific concern that pollution, in addition to incidental catches of dolphins
by the tuna fishing industry, may threaten dolphin populations. Pathological examination
of dolphins stranded in 1987 suggest a chronic immune system suppression. This could
have been a consequence of sublethal exposure to a red tide and/or a consequence of
unusually high concentrations of PCBs in the dolphin tissues. In addition, recent
"epidemics" of a distemper-like virus have caused mass mortalities among several
populations of seals. Some suspect that coastal pollution has increased the seals'
susceptibility to the virus, but the cause of the outbreaks is as yet undetermined.
Unusually warm temperatures also may contribute to outbreaks of the .virus.
In addition to mass mortality events, many pinniped (i.e., seals, sea lions, and
walruses) populations have been declining recently. Bioaccumulation of PCBs or other
toxic substances are known to reduce reproductive success in seals, and may be
contributing to these population declines in some areas.
IX
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Forests worldwide. Forests are declining and being damaged worldwide. In the
tropics, clearing land for agriculture and other land uses is the most significant problem,
whereas in the north temperate zone, forest dieback resulting from atmospheric pollution
is an additional problem.
Clearing of tropical rainforest is proceeding at an unprecedented rate that could
result in the complete loss of such forests by the year 2050. In North America,
deforestation and reforestation are more balanced; however, old growth forests are at
risk of being lost completely in the Pacific Northwest.
Beyond the conclusion that general atmospheric pollution is leading to north
temperate forest dieback in the developed countries, researchers have not been able to
identify a more specific common cause across the continents. Because multiple
pollutants are generally present in the forests of concern, attribution of forest dieback to
specific direct or indirect effects of acid rain, ozone, or other atmospheric sources of
pollution remains controversial. Current evidence implicates a variety of natural biotic
and abiotic stresses upon which are superimposed physical and chemical stresses of
anthropogenic origin that may have originated long distances from the affected sites.
Summary. Available evidence indicates that human activities are contributing to
many of the observed population declines described in this report. The direct
destruction, degradation, and fragmentation of habitats as lands and waters are converted
and altered for human use appear to be the major contributors to declines in populations
of neotropical songbirds, ducks, freshwater fish, and land turtles in North America. It is
not yet clear whether the apparent decline in amphibian populations worldwide is real,
and if so, what the cause(s) of the trend might be. Increasing environmental pollution is
taking its toll on the surface water quality upon which our fish fauna depend, and may
have contributed to the recent deaths and declines of dolphins and seals in the North
Atlantic and the Mediterranean. Our deliberate and inadvertent introduction of non-
native species of fish, frogs, and other organisms also has had a devastating effect on the
diversity and abundance of our native fauna and flora. In addition to suffering from
physical destruction, nutrient runoff and sedimentation, and pollution, coral reef
communities may be suffering directly from a global ocean warming trend or increased
variability in ocean temperatures. The clearing of tropical rainforests not only threatens
global biodiversity, but also the services supplied by those forests in stabilizing our global
climate.
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AUTHORS, CONTRIBUTORS, AND REVIEWERS
The U.S. Environmental Protection Agency's Office of Policy, Planning and
Evaluation sponsored this report, with D. Eric Hyatt serving as editor and Otto Gutenson
serving as associate editor. Dr. Margaret McVey, a consultant, was the principal author.
Tom Born of the Office of Policy, Planning and Evaluation developed many of the report
figures. This document was prepared under EPA Contract No. 68-W9-0080.
AUTHORS
D. Eric Hyatt, Editor
Office of Policy, Planning and Evaluation
U.S. Environmental Protection Agency
Washington, DC
Dr. Margaret McVey, Principal Author
ICF Incorporated
Fairfax, VA
Otto Gutenson, Associate Editor
Office of Policy, Planning and Evaluation
U.S. Environmental Protection Agency
Washington, DC
Tom Born, Contributing Author
Office of Policy, Planning and Evaluation
U.S. Environmental Protection Agency
Washington, DC
CONTRIBUTORS
Cathy Richardson
American Fisheries Society
Bethesda, MD
Dr. Roy McDiarmid
American Museum of Natural History
New York, NY
Dr. Richard Montali
National Zoological Park
Washington, DC
Dr. Dexter Hinckley
Office of Policy, Planning and Evaluation
U.S. Environmental Protection Agency
Washington, DC
Donna Johnson
National Wildlife Federation
Washington, DC
Dr. Michael Klemens
American Museum of Natural History
New York, NY
Dr. John Carr
Conservation International
Washington, DC
XI
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REVIEWERS
Dr. Ernest H. Williams, Jr.
Department of Marine Sciences
University of Puerto Rico, Lajas, PR
Dr. William A. Dunson
Department of Biology
Pennsylvania State University
University Park, PA
Dr. Kim Devonald
Office of Policy, Planning and Evaluation
U.S. Environmental Protection Agency
Washington, DC
Dr. Sally Valdes-Cogliano
Office of Policy, Planning and Evaluation
U.S. Environmental Protection Agency
Washington, DC
Dr. Richard L. Wyman
Edmund Niles Huyck Preserve, Inc.
Biological Research Station
Rensselaerville, NY
Jamie K. Doyle
Smithsonian Migratory Bird Center
National Zoological Park
Washington, DC
Dr. Jay J. Messer
Science Advisor to
Senator Daniel P. Moynihan
Washington, DC
Christopher R. Solloway
Office of Policy, Planning and Evaluation
U.S. Environmental Protection Agency
Washington, DC
Cover illustration by Kimberly Hall, University of Michigan.
Xll
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DISCLAIMER
Although the information in this document has been funded wholly of in part by the
United States Environmental Protection Agency, it does not necessarily reflect the views
of the Agency and no official endorsement should be inferred.
xm
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1. OVERVIEW OF BIOLOGICAL POPULATIONS AS
INDICATORS OF ENVIRONMENTAL CHANGE
We live in a era of unprecedented loss of biological diversity and possibly life-
supporting services provided by ecosystems (Myers, 1988; Wilson, 1989). The human
population on the planet has more than doubled since 1954 (Mostafa, 1989). An
estimated 25 percent of the world's species present in the mid- 1980s may be extinct by
the year 2015 or soon thereafter (Raven 1988a,b). Various ecosystem services, such as
the regulation of water discharge, soil generation, and the absorption and breakdown of
pollutants, are being degraded in some areas as component species vanish from these
ecosystems or as natural habitats are converted to other land uses (Reid and Miller,
1989). Our lives also are being
impoverished by the loss in many areas of
components of our planet's ecosystems
that we have taken for granted in the
past: hearing the song of a wood thrush
in the spring, snorkeling to view coral reef
communities, or spending a day outdoors
fishing or hunting waterfowl.
Dead Mediterranean
Dolphins Give Nations
Pause (Washington Post,
1992)
The loss of biodiversity and
ecosystem services as a whole are difficult concepts to grasp, and may not allow us to
visualize easily how human activities impinge on the biological health of our planet. It
may be easier for us to think in terms of specific indicators of changes, such as a decline
in bird species that we can identify during
spring and fall migrations or the failure of
frogs to return to ponds in our favorite
hiking areas. We are shocked to read of
hundreds of dolphins found dead and
dying on our Atlantic beaches, and
wonder not only what has happened to
these creatures, but also what the event
may portend for our own future and well-
being. Within the last decade, the frequency with which the news media (e.g., The
Washington Post, The New York Times) have identified such occurrences has increased,
and now can be found almost monthly. This frequency of reporting on such occurrences
reflect the number of recent reports in the scientific literature.
From Minnow to Sturgeon,
North American Fish are
in Peril (NY Times, 1990)
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But what do these changes really mean? Which are natural occurrences in
response to variability in weather or other natural phenomena, and which are
consequences of man's activities? We may wonder what these phenomena tell us about
the condition of our environment. Which of man's activities are the most damaging to
our biological heritage, and what, if
anything can we do to reverse these
losses? Which of these changes or
indicators would be most representative of
environmental conditions?
Coral Reefs Off 20 Countries
Face Assaults from Man and
Nature (NY Times, 1990)
1.1. Selection of Indicators:
Technical and Popular Literature Scan
Different groups of organisms are vulnerable to different aspects of man's
activities and the changes wrought on the environment by those activities. The health
and welfare of "indicator" populations of organisms might serve as a barometer of
different aspects of our changing environment and harbingers of consequences yet to
come. As part of their strategic planning, the US Environmental Protection Agency's
(US EPA) Environmental Results Branch (ERB) initiated an investigation into these
phenomena in an attempt to determine which, alone or in combination, might serve as
indicators of general environmental change at regional, continental, hemispheric, or
global scales. ERB recognized that there are a number of potentially important
environmental indicators outside those areas being considered by EPA's program offices
(e.g., Office of Air and Radiation, Office of Water, etc.), indicators that might reflect the
cumulative effects of human disturbances
on many different components of our
environment (e.g., water, soil, air).
This report is based on an initial
literature scan to identify and evaluate
potentially useful ecological indicators of
Loss of Tropical Forests is
Found Much Worse than was
Thought (NY Times, 1990)
environmental quality. This included a
review of popular literature to identify
those phenomena that have caught the
public's attention and of the scientific
literature to determine the validity of the
reported trends and what is known about
natural and anthropogenic causes of these
trends. The phenomena selected for this
report are not necessarily considered of
Frogs, Toads Vanishing
Across Much of the World;
"Environmental
Degradation" May be to
Blame, Scientists Say
(Washington Post, 1990)
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greater importance by the scientific community than a number of biological phenomena
not discussed here. But they appear to be of at least some concern to the public as
indicated by the news scan. Therefore conducting a technical literature review to present
the current state of scientific knowledge about these phenomena should serve a useful
purpose in addressing the interests of our "customers", the public, in knowing more about
the possible implications of the phenomena. Of the twelve topics that received the most
coverage recently in the popular press (Exhibit 1), loss of biodiversity and loss of wetland
habitats are the focus of major EPA research efforts and a number of other reports, and
will not be covered in this volume. This report focuses on eight of the remaining ten
topics. These eight topics were chosen based on scientific merit, quality of information
available, and breadth of geographic scope. The remaining two topics (decrease in
shellfish populations and increasing incidence of algae blooms) and other potential topics
are not discussed in this report but may be addressed in future volumes.
This report summarizes the findings of the literature review in three sections. The
remainder of Section 1 describes the literature review and acquisition strategy and
identifies several potential biological indicators of environmental change. In Section 2,
we describe each of the eight phenomena selected for review separately. For each, we
describe level of applicability (e.g., regional to global), recent trends in the indicator,
current hypotheses on the cause(s) of the
observed trends, and the evidence
available to support each hypothesis. In
Section 3, we present an overview of all
eight trends, and what they indicate
concerning the impacts of human activities
on environmental quality.
Seen any Warblers Lately?
(NY Times Magazine,
1990)
1.2. Methods
To identify literature pertaining to biological populations as potential indicators of
environmental change, we conducted a screen-level online computer search of popular
and scientific literature and contacted academic experts and other professionals and
organizations known to be involved in research or publications concerning biological
trends (see Acknowledgements). Using these
approaches, we identified several potentially
important population indicators of
environmental change at regional, national,
hemispheric, and global levels, that had
received attention in the popular press in
recent years. We selected eight of the twelve
topics that not only receive heavy academic
and popular press coverage, but also appear
to exhibit the most technical merit and wide
Their Beaches Eroding,
Threatened Sea Turtles Have
Few Places to Nest (NY
Times, 1992)
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Exhibit 1. Biological populations as potential indicators of environmental change.
Addressed in This Report
(1) Declining populations of neotropical migrant birds;
(2) Declining populations and increasing numbers of extinctions of North
American fish species;
(3) Decreasing populations of North American ducks;
(4) Increased incidence of coral bleaching, degradation, and death worldwide;
Preliminary Review in This Report
(5) Declining populations of amphibians worldwide;
(6) Decreasing populations of turtles worldwide;
(7) Mass deaths of dolphins and seals and declining populations of seals;
(8) Loss of forests worldwide and forest "dieback" in the north temperate
zones;
Not Addressed in this Report
(9) Increasing incidence of brown algal blooms and concurrent die-offs of
marine animals;
(10) Decreasing populations of shellfish from pollution and disease;
(11) Continued loss of wetlands in North America; and
(12) Loss of biodiversity worldwide.
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ygeographic scope. We then conducted a thorough search of the scientific literature of
the eight topic areas which are the focus of this report. This report, therefore, is a
scientific review of the technical literature, with the selection of indicators influenced in
part by public perceptions of potential importance as well as by scientific concerns.
1.3. References
Mostafa, T. 1989. Our biological heritage under siege. BioScience 39:725-728.
Myers, N. 1988. Essay: Tropical-forest species: going, going, going... Scientific
American, 259:132.
Raven, PH. 1988a. Biological resources and global stability. In: Kawano, S., Connell,
JH, and Hidaka, T (eds.) Evolution and coadaptation in biotic communities. Tokyo,
Japan: University of Tokyo Press, pp. 3-27,
Raven, PH. 1988b. Our diminishing tropical forests. In: Wilson, EO, and Peter, FM
(eds.) Biodiversity. Washington, DC: National Academy Press, pp. 119-122.
Reid, WV, and Miller, KR. 1989. Keeping options alive: The scientific basis for
conserving biodiversity. Washington, DC: World Resources Institute.
Wilson, EO. 1989. Threats to biodiversity. Scientific American 260:108-116.
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2. SYNOPSIS OF EIGHT POTENTIAL BIOLOGICAL
POPULATION INDICATORS
In this section, we provide a synopsis of eight potential biological indicators of
large-scale environmental change for ERB (Exhibit 1, Indicators number 1 though 8).
We have focused more effort on the first four indicators (i.e., neotropical migrant birds,
North American freshwater fish, North American ducks, coral reefs worldwide) because
they appear to be more promising in the short-term as indicators of environmental
change. These four potential indicators were included in EPA/OPPE's 1992 report on
Strategies, Goals, and Environmental Results. They represent groups for which there is
strong evidence linking specific types of environmental change with population trends.
Three of the remaining four indicators (i.e., amphibians, turtles, and dolphins and seals)
also show potential as indicators, but either clear trends or links have not yet been
established or the trends result from a combination of many different problems. Loss
and degradation of forests currently is receiving attention by numerous organizations, and
is reviewed here because of its fundamental relationship to several of the other potential
indicators.
For each potential indicator included in this section, we first summarize our
findings. We then provide a brief background of the organism group and describe the
recent trends or events for each group, e.g., declining populations, increased incidence of
disease. We then review current hypotheses explaining the trends, available evidence in
support of the trends, consensus of the scientific community on the hypotheses, and when
possible, the relative magnitude of each cause's contribution to the trends. We conclude
each section with a reference list and a bibliography of articles that have appeared
recently in the popular press.1
2.1. Neotropical Migrant Bird Species
Summary. Fragmentation of North American forests is contributing to the decline
of neotropical migrant bird species that breed in forest interiors. Forest fragmentation
exposes larger proportions of the remaining forest to edge conditions and edge predators
and parasites, and several characteristics of neotropical migrant species make them more
vulnerable to these changes than short-distance migrants or resident species. The relative
contribution of "island effects" of forest fragmentation to the decline of neotropical
migrants on a regional scale has not been analyzed.
**P following a citation year indicates that the reference is found in the Popular Press Bibliography
section rather than in the Reference section.
-------
Tropical deforestation also might be contributing to the observed population
declines of neotropical migrant species, but scientists do not agree on this issue.
Whether or not tropical deforestation currently is contributing to the declining
neotropical migrant bird populations, it is likely to become a more serious problem than
fragmentation of habitat in North America in the hear future. Obviously, continuing
tropical deforestation and North American forest fragmentation are likely to cause
continued population losses of neotropical migrant species.
2.1.1. Description
Background. Neotropical migrants are those species that breed mainly in the
temperate region of North America and winter mainly south of the Tropic of Cancer in
the Western Hemisphere (Terborgh, 1989). Of the bird species of the contiguous United
States, 332 species (51 percent) migrate annually to the neotropics (Lovejoy, 1983). In
large tracts of mature eastern deciduous forest, as many as 70 to 90 percent of the
breeding birds are neotropical migrants (Terborgh, 1989; Whitcomb et al., 1979). This is
because most forest-interior breeding birds are insectivorous and must follow the warm
temperatures associated with their food supply. Exhibit 2.1.1 illustrates the migratory
pathways of these birds.
Trends. Populations of many neotropical migrant bird species have reportedly
been declining over the past 20 to 40 years (Aldrich and Robbins, 1970; Ambuel and
Temple, 1982; Anderson, 1979; Askins and Philbrick, 1987; Briggs and Criswell, 1979;
Butcher et al., 1981; Hall, 1984; Holmes and Sherry, 1988; Jones, 1986; Leek et al., 1988;
Robbins, 1979; Serrao, 1983, 1985; Temple and Temple, 1976; Walcott, 1974; Whitcomb
et al., 1981); however, most studies have concerned local populations, and the reported
findings might have been unique to
those particular sites (Hutto, 1988).
Recent data analyses for the entire
eastern region of North America
indicate that most neotropical migrant
bird species that breed
in forest interiors of the
eastern United States and Canada
have recently (1978-1987) declined
in abundance after a period of
stable or increasing populations
(Exhibit 2.1.2; Robbins et al., 1989).
Between 1966 and 1978, increasing
breeding population sizes were
observed in 76 percent of neotropical
migrant species (based on the US
Fish and Wildlife Service (FWS)
Breeding Bird Survey; Robbins et al.,
Blackburnian warbler (artist Kimberly Hall)
-------
Exhibit 2.1.1. Migratory pathways of neotropical songbirds.
Neotropical migrant songbirds leave their breeding grounds in the United States and Canada
to winter in subtropical and tropical areas of Central and South America.
Source: Greenberg, 1989.
8
-------
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1989). In contrast, between 1978 and 1987, negative trends were observed in 71 percent
of the species (Robbins et al., 1989). The fact that populations of most permanent
resident and short-distance migrant bird species are not declining supports the hypothesis
that phenomena unique to the neotropical migrants are at issue (Robbins et al., 1989;
Terborgh, 1989).
2.1.2. Hypotheses
The decline of neotropical migrant bird species was initially perceived as a "forest
fragmentation effect" in North America (Terborgh, 1989). Several species appeared to
be "area sensitive", i.e., they could only be found in large tracts of forest and were absent
from small patches of forest (Askins et al., 1987; Howe, 1984; Robbins, 1980; Terborgh,
1989). As forests continued to be fragmented by human activities and suburban
developments, fewer forest tracts were sufficiently large to accommodate the "area
sensitive" species. By the late 1970's, the area-sensitive forest-interior species recognized
by Whitcomb et al. (1979) included not only the yellow-billed cuckoo, wood thrush, red-
eyed vireo, black-and-white warbler and scarlet tanager recognized by Galli et al. (1976),
but also the whip-poor-will, pileated woodpecker, Acadian flycatcher, veery, yellow-
throated vireo, worm-eating warbler, northern parula warbler, ovenbird, Louisiana
waterthrush, Kentucky warbler, hooded warbler, and American redstart (Robbins, 1979).
Given the rate of tropical deforestation by the early 1980's, concern also developed over
the loss of wintering habitat (Morse, 1980; Terborgh and Winter, 1980; Terborgh, 1989).
We review the evidence available to support the hypotheses of breeding forest
fragmentation and loss of wintering habitat in the tropics in Sections 2.1.2.1 and 2.1.2.2,
respectively.
2.1.2.1. Forest fragmentation and loss of breeding habitat in North America
Causes of forest fragmentation include suburban development, super highways,
transmission lines, reservoirs, and surface mining (Robbins, 1979). Many studies have
indicated that fragmentation of forests adversely affects forest-interior species (Askins et
al., 1987; Howe, 1984; Lynch and Whitcomb, 1978; Lynch and Whigham, 1984; Robbins,
1979; Whitcomb et al., 1981). Many species of neotropical migrants are found
predominantly in large tracts of continuous forests and are found in much lower densities,
or not at all, in isolated forests (Howe, 1984; Robbins, 1980; Terborgh, 1989). Recently,
Faaborg and Arendy (1989) provided evidence supporting the hypothesis that problems
in the North American forests are responsible for at least some of the declines. They
found that the number of wintering migrants captured in the Guanica Forest of Puerto
Rico between 1973 and 1988 has been steadily declining, even though this tropical forest
is protected and has not appeared to change in vegetation or resident bird species over
this time (Exhibit 2.1.3). Other evidence in support of this hypothesis comes from a 10-
year investigation in the Hubbard Brook Experimental Forest in New Hampshire. Sherry
and Holmes (1992) found that breeding populations of American redstarts in Hubbard
Brook were significantly correlated with the previous year's fledging success regardless of
10
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how the population fared on their wintering grounds. Two major hypotheses have been
offered to explain the sensitivity of the neotropical migrants to forest fragmentation in
their breeding habitat: edge effects and island effects, as discussed below.
Edge effects. Forest fragmentation increases the ratio of forest edge to forest
interior. Surveys of nesting success in North American deciduous forests indicate that
nesting success is lower near the forest edge and in small forest patches than in the
interior of large forests (Askins et.al., 1990). For example, in Wisconsin, Temple and
Gary (1988) found that nest success of 13 species was 70 percent in areas greater than
200 m from the forest edge (n = 82 nests); 58 percent in areas 100 to 200 m from the
edge (N = 98); and only 18 percent in areas less than 100 m from the edge (n = 96).
Forest edges support several generalist species of predators (e.g., bluejays, raccoons) that
are absent or rare in forest interiors, as well as the brown-headed cowbird, which
parasitize other birds nests. We review evidence that increased nest predation and
parasitism rates account for the reduced nesting success at forest edges in the following
paragraphs.
The abundance of some nest predators, such as the blue jay, American crow, and
raccoon, have increased over the past few decades in areas of human disturbance
(Terborgh, 1989; Wilcove, 1985b) and are more common along forest edges than in
forest interiors (Terborgh, 1989). Using artificial nests supplied with quail eggs, Wilcove
(1985a) demonstrated that nests located at forest edge experience higher predation rates
than nests located in forest interior. Wilcove (1985a) also found that the percentage of
nests preyed upon increased as the size of a forest patch decreased, to levels ranging
from 30 to 95 percent in forests approximately 5 acres in size (Exhibit 2.1.4). In contrast,
he found only 2 of 100 nests set out hi the Great Smoky Mountains National Park to be
raided. Similar results have been obtained using artificial nests in Maine (Small and
Hunter, 1988) and Pennsylvania (Yahner and Scott, 1988).
Forest edges also support the brown-headed cowbird, a nest parasite of open and
edge habitats that lays its eggs in the nests of other bird species (Brittingham and
Temple, 1983; Bystrak and Robbins, 1977; Mayfield 1977a; Terborgh, 1989; Wilcove,
1985a,b; Whitcomb et al., 1981). Cowbirds forage in open fields, but female cowbirds
concentrate host-searching activities along forest edge and may penetrate into the forest
several hundred meters while searching for nests (Brittingham and Temple, 1983;
Rothstein et al., 1984). Exhibit 2.1.5 indicates that cowbird parasitism can reach as far as
300 meters or more into the forest interior. The cowbird young hatch earlier than the
host young and, being larger and noisier, get most of the food brought to the nest. As a
result, fewer than normal, or often none, of the host's young fledge from a parasitized
nest (Payne, 1977; Mayfield, 1977a,b; as cited in Brittingham and Temple, 1983). Forest-
interior breeding species that have not coevolved with open habitat parasites such as
cowbirds lack effective defense mechanisms (e.g., evicting the parasite's egg) (Rothstein,
1975).
11
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Exhibit 2.13. Decline in the number of winter resident warblers captured at the
Guanica Forest, Puerto Rico, between 1973 and 1988.
a.
(3
•s
I
D>
30
25
20
15
•g 10
1
3 -
73
75
77
79 81
Year
83 85 87
The number of vfinter resident warblers captured each year in a protected forest in Puerto Rico
declined significantly between 1973 and 1988, despite no obvious change in the forest over that
time. The dots are the number of captures in 16 nets during 14 three-day samples each year. The line is
a representation of the trend that statistically best describes the data.
Source: Faaborg and Arendy, 1989.
12
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Exhibit 2.1.4. Increase in percentage of nests preyed upon with decreasing forest
fragment size.
100 -
O
75 -
2>
Q.
tt 50 -H
8
I
25 -
20 20
•O
13
20
44
40
50
I
10
T
T
100 1,000 10,000
Forest Fragment Size (hectares)
I
100,000
Nest predation is highest in the smallest forest fragments. Closed squares are large forest tracts,
open circles are rural fragments, and closed circles are suburban fragments. The number above each point
is the number of artificial nests placed in that forest. Since the experimental nests may be more
conspicuous than natural nests, this experiment provides only a relative, not absolute, indication of
predation rates with distance from the forest edge.
Source: Wilcove, 1985a.
13
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Exhibit 2.1.5. Decreasing incidence of cowbird parasitism with increasing distance from
forest openings.
100 -
75 -
S
CO
n.
tn
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CD
U
I
50 -
25 -
65%
',.; •••*
sji-Mpfty
<:^
46%
36%
18%
0-99
100-199
200-299
>300
Distance to Forest Opening/Edge (m)
Cowbird parasitism is highest at the forest edge; but is evident up to 300 meters into the forest
interior. Cowbirds are the principal North American species of bird that parasitizes other
birds by placing eggs in their nests. Some host species, such as robins, catbirds, and bluejays,
recognize the cowbird eggs as alien and dispose of them. Almost all neotropical migrant
species, however, do not distinguish a cowbird egg from their own and will feed a young
cowbird as their own. This results in far fewer of the host species'young surviving because the
cowbird egg tends to hatch first and, being larger and noisier than the hosts' own offspring, the
young cowbird gets most of the food brought to the nest. The hosts' own young often starve or
are crowded out. Analysis is limited to forest openings greater than 0.2 hectares. Host species were
predominantly neotropical migrants: Acadian flycatcher (37 nests), wood thrush (N = 15), veery (N = 5),
ovenbird (N = 15), hooded warbler (N = 4), least flycatcher ( N = 5), red-eyed vireo (N = 1), American
redstart (N = 4), mourning warbler (N = 1), Louisiana waterthrush (N = 1), scarlet tanager (N = 2),
indigo bunting (N = 10), and rose-breasted grosbeak (N = 5).
Source: Brittingham and Temple, 1983.
14
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Brown-headed cowbirds have increased dramatically in numbers and geographic
range in the current century. As shown in Exhibit 2.1.6, the percent of Audubon
Christmas Bird Count records that include the cowbirds has risen from less than 1
percent at the turn of the century to over 80 percent by 1980 (Brittingham and Temple,
1983). In 1985, the shiny cowbird, a brood parasite originally confined to South America
and nearby islands (Perez-Rivera, 1986), reached the United States and has been
expanding its range in Florida (Smith and Sprunt, 1987).
Many neotropical migrant bird populations are experiencing high levels of brown-
headed cowbird parasitism (Terborgh, 1989), and, in some areas, virtually all nests of a
species are successfully parasitized (Terborgh, 1989). The endangered Kirtland's warbler
(Dendroica kirtlandii) provides a dramatic example of the potential magnitude of cowbird
effects on a neotropical migrant species. Kirtland's warblers breeding habitat is restricted
to Jack pine forests in central Michigan (Botkin et al., 1991). When cowbirds had
unrestricted access to Kirtland's warbler nests, the warblers could not produce enough
young to offset normal mortality (Walkinshaw, 1983; as cited by Terborgh, 1989). The
existing populations of Kirtland's warbler declined by 60 percent from 1961 to 1971,
apparently because of a high incidence of cowbird parasitism (i.e., up to 83 percent of all
nests). With nest parasitism, the warblers fledged less than one young per nest.
Beginning in 1972, cowbirds were trapped and removed annually from the warbler's
breeding habitat, and parasitism rates dropped to below five percent (Kelly and
DeCapita, 1982). With little nest parasitism, the warblers fledged nearly three young per
nest, and the population has stabilized, although it is not increasing as had been hoped
(Kelly and DeCapita, 1982; Mayfield 1977a,b; as cited by Brittingham and Temple 1983).
Cowbird trapping programs also are being tried elsewhere (Beezley and Rieger, 1987;
Wiley et al., 1991).
Susceptibility of neotropical migrant species to edge effects. Several life-history
characteristics make the neotropical migrant species more susceptible to increased nest
predation and parasite pressure than resident or short-distance migrant species (Askins
and Philbrick, 1987; Lynch and Whigham, 1984; Robbins, 1979; Terborgh, 1989;
Whitcomb et al., 1979; Wilcove, 1985a). Neotropical migrant species:
are obligate inhabitants of forests (i.e., live only in forests);
nest on or near the ground;
tend to build open nests;
raise only a single brood of young per year;
have comparatively small clutch size; and
have no defense mechanism against cowbirds.
Birds that reproduce successfully at forest edges have the following qualities (Lynch and
Whigham, 1984; Robbins, 1979):
15
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Exhibit 2.1.6. Increase in cowbird abundance in the United States from 1900 to 1980.
I
o
O
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Si1
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=3 O
80 -
60
40
20
. *
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• • •mmm
• i ' 1 L
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1900
1920
1940
1960
1980
Year
Brown-headed cowbirds, the principle parasitic bird species in North America, have increased
sharply in numbers and geographic range in the United States since 1900. Based on Audubon
Christmas Bird Counts.
Source: Brittingham and Temple, 1983.
16
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are permanent residents or short-distance migrants;
nest higher above the ground;
build nests in protected cavities;
often raise two or more broods per season;
have relatively larger clutches; and
may recognize a cowbird egg and eject or otherwise avoid it.
Because edge effects (i.e., increased nest predation and parasitism) can extend more than
three hundred meters into a forest (Brittingham and Temple, 1983), areas in which forest
fragments are only several hundred meters in width provide no true forest interior. Thus,
none of the forest in many fragmented landscapes may be suitable for neotropical
migrant birds that breed in forest interiors.
Island effects. MacArthur and Wilson's (1963, 1967) theory of island biogeography
is relevant to understanding impacts of forest fragmentation on neotropical migrant birds.
This theory states that the low species diversity characteristic of oceanic islands reflects a
dynamic equilibrium, or balance, between rates of extinction and rates of colonization of
individual species populations. The number of animal species found on a particular
island at equilibrium is thought to depend on the island's productivity, its microhabitat
diversity (e.g., variation in vegetation, topography, climate), and its size and degree of
isolation from sources of potential colonists (as summarized by Whitcomb et al., 1979).
Forest loss and fragmentation has resulted not only in smaller patches of
"undisturbed" forests, but also in increasing isolation of the forest "islands." As forest
islands become more isolated from one another, locally rare species may become more
vulnerable to local extinctions as a consequence of natural variation in mortality rates
and reproductive success (Diamond, 1984; Howe, 1984; Terborgh, 1980; Terborgh and
Winter, 1980; Whitcomb et al., 1979). Several studies have demonstrated that when a
large forest is reduced in size, bird communities typically experience declines in species
numbers (Ambuel and Temple, 1983; Butcher et al., 1981; Forman et al., 1976; Galli et
al., 1976; Howe, 1984; Lynch and Whigham, 1984; Moore and Hooper, 1975; Robbins,
1980; Terborgh, 1989; Whitcomb et al., 1977; Whitcomb et al., 1981) and in breeding
densities (Aldrich and Coffin, 1980; DellaSala and Rabe, 1987; Howe, 1984; Lynch and
Whigham, 1984; Robbins, 1979, 1980). Robbins (1980) illustrated how the occurrence of
neotropical migrant species increases with increasing forest patch size (Exhibit 2.1.7).
Species such as the wood thrush, eastern wood pewee, and red-eyed vireo were found in
most woodlands more than 20 hectares in size; the pileated woodpecker, Acadian
flycatcher, blue-gray gnatcatcher, and worm-eating warbler were not found in any woods
of less than 17 hectares (Exhibit 2.1.7). Thus, it may even be possible to develop "stress-
response" curves to predict the effects of continued forest fragmentation on various
species of neotropical migrants.
17
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Exhibit 2.1.7. Proportion of woodlands of each size class in which the species indicated
were found in the District of Columbia or Maryland.
100
•8 80
c
60
QL 40
20
Wood Thrush ^—~r«Tx"
" / '
X
*
Scarlet Tanager
Red-eyed Vireo
Pileated Woodpecker,
Acadian Flycatcher,
and
Blue-gray Gnatcatcher
/
Worm-eating Warbler
3-6 7-17 21-31 36-102 120-1300 4000
Hectares
The probability of finding given neotropical migrant bird species in a woodland increases with
increasing size of the woodland. Also, more species are found in the larger woodlands.
Source: Robbins, 1980. The figure is based on the work of Briggs and Criswell, 1979; Lynch and
Whitcomb, 1978; Galli et al., 1976; and data that Robbins collected in Maryland since 1951.
18
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Other hypotheses. Another hypothesis to explain forest fragmentation effects
considered by several investigators is that neotropical migrants may be competitively
replaced by other species due to changes in habitat structure (Anderson, 1979; Aldrich
and Coffin, 1980; Butcher et al., 1981; Ambuel and Temple, 1983; and Askins and
Philbrick, 1987, as cited in Hutto, 1988). The necessary competitive exclusion
experiments, however, have not been performed and would be very difficult (Terborgh,
1989). Moreover, none of the available evidence points strongly in this direction
(Terborgh, 1989).
2.1.2.2. Loss of wintering habitat in the tropics
Several researchers have suggested that the recently increasing rates of tropical
deforestation and consequent loss of wintering habitat for the neotropical migrants is
responsible for the observed population declines (Ambuel and Temple, 1982; Briggs and
Criswell, 1979; Hall, 1984; Howe, 1984; Lovejoy, 1983; Rappole et al., 1983; Terborgh,
1980). Morton and Greenberg (1989) reported that the rate of forest conversion in the
neotropics ranges from one to four percent per year. This rate of change is "too great to
allow for genetic adaptations of its [native bird species] through natural selection"
(Morton and Greenberg, 1989).
The evidence for this hypothesis has been controversial, with some investigators
finding no evidence of tropical deforestation effects (Holmes et al., 1986; Holmes and
Sherry, 1988; Hutto, 1988; Wilcove, 1988), others finding no alternative explanation for
the observed declines (Hall 1984; Leek et al., 1988; Marshall, 1988), and still others
admitting that the evidence is suggestive, but not yet conclusive (Lovejoy, 1983; Wilcove
and Terborgh, 1984; Terborgh, 1989).
Neotropical migrants have large breeding ranges in comparison to their small
wintering ranges (i.e., winter densities are much higher than breeding densities) (Hall
1984; Morton and Greenberg, 1989). Terborgh (1989) has estimated on this basis that
one acre of tropical forest may be equivalent to five to ten acres of north temperate
forest. Wilcove and Terborgh (1984) suggested that the amount of habitat available in
North America and in the wintering habitats was in balance in pre-colonial times.
Initially, deforestation proceeded most rapidly in the north temperate zone.
Subsequently, tropical deforestation rates increased (see Section 2.8). The ratio of
summer and winter habitats may again be in balance, but the trend for the future will be
of decreasing availability of forested wintering habitat in the tropics relative to breeding
habitat in the north temperate zone. Several different patterns of population decline are
possible under these circumstances, and Wilcove and Terborgh (1984) suggest that it may
be unreasonable to expect unanimous agreement among investigators as to cause and
effect at the early stages of species' decline.
Recently, however, using data from the US Fish and Wildlife Service (FWS)
Breeding Bird Survey, Robbins et al. (1989) has provided strong evidence that tropical
19
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deforestation is contributing to a regional decline of neotropical migrant species. To
avoid potential data biases associated with changing breeding habitat distributions in
North America (e.g., increasing forest cover in New England, decreasing forest cover in
the southeast), they compared population trends of neotropical migrants that overwinter
in forested areas with those that overwinter in scrub habitats in the tropics. They found
larger declines for the forest-wintering species than for the scrub-wintering species, many
of which are in fact increasing in abundance. Robbins et al. (1989) concluded that in the
last decade, tropical deforestation may be having a greater impact on neotropical
migrants than is loss and fragmentation of forest habitats in North America.
2.13. Continued Monitoring
A variety of groups and organizations monitor bird populations, but the most
comprehensive surveys in the United States are sponsored by the Audubon Society, the
US FWS, and Cornell University.
The National Audubon Society sponsors three bird censuses: (1) the Christmas
Bird Count, which started in 1900, (2) the Breeding Bird Census, which started in 1937,
and the Winter Bird-Population Study, which started in 1947/48.
• The Christmas Bird Counts are conducted by tens of thousands of volunteers
annually (Brody, 1989*P). Groups of bird watchers count all of the birds that they
see in a day. The protocol is not scientific, and potential biases toward
overcounting and misidentification cannot be ruled out. Moreover, the ratio of
birds seen to birds present depends on many uncontrolled variables such as
weather, observer density, duration and timing of observation periods, and
variation in observer skills. Recently, the National Audubon Society has instituted
more stringent counting rules and data checks to help counter biases (Brody,
1989*P).
• The Breeding Bird Census is a monitoring program in which the density of
territorial males is estimated on a plot of homogeneous habitat. The vegetation in
the plot also may be sampled (Temple and Wiens, 1989). Again, the protocol is
not scientific, and some biases may result.
• The Winter Bird-Population Study is the winter analogue of the Breeding Bird
Census, but the bird-habitat data have not been used extensively (Temple and
Wiens, 1989). Due to the volunteer nature of the data collection effort, biases
may be present in the data.
The US FWS Breeding Bird Survey (BBS), established in 1966, is an annual
roadside survey of United States and Canadian birds. The surveys are conducted each
June along approximately 2,000 roadside "routes." Experienced volunteers recruited by
state and provincial coordinators sample bird populations at 50 stops at 0.8-km intervals
20
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along secondary roads. This survey relies upon singing males, however, which may
constitute only a fraction of the total male population. Nonbreeding "floaters" may be an
important component of the population (Morton and Greenberg, 1989). Thus, the FWS
Breeding Bird Surveys may not show a population decrease when one is really occurring,
which makes the recent results of the BBS even more dramatic.
The Cornell Laboratory of Ornithology manages several computerized databases
on North American birds, including the North American Nest Record Program, the
Colonial Bird Register, and two new programs, Project Birdwatch and Project
FeederWatch. In addition, the Cornell Laboratory maintains the computerized databases
for Audubon's three survey programs (Temple and Wiens, 1989).
2.1.4. References
Aldrich, JW, and Robbins, CS. 1970. Changing abundance of migratory birds in North
America. Smithsonian Contr. Zool. 26:17-26.
Aldrich, JW, and Coffin, RW. 1980. Breeding bird populations from forest to suburbia
after 37 years. Am. Birds 34:3-7.
Ambuel, B, and Temple, SA. 1982. Songbird populations in southern Wisconsin forests:
1954 and 1979. J. Field. Ornithol. 53:149-158.
Ambuel, B, and Temple, SA. 1983. Area-dependent changes in the bird communities
and vegetation of southern Wisconsin forests. Ecology 64:1057-1068.
Anderson, SH. 1979. Changes in forest bird species composition caused by
transmission-line corridor cuts. Am. Birds 33:3-6.
Askins, RA, Philbrick, MJ, and Sugeno, DS. 1987. Relationship between the regional
abundance of forest and the composition of forest bird communities. Biol. Conserv.
39:129-152.
Askins, RA, and Philbrick, MJ. 1987. Effect of changes in regional forest abundance on
the decline and recovery of a forest bird community. Wilson Bull. 99:7-21.
Beezley, JA, and Rieger, JP. 1987. Least Bell's vireo management by cowbird trapping.
Western Birds 18:15-61.
Botkin, DB, Woodby, DA, and Nisbet, RA. 1991. Kirtland's warbler habitats: A
possible early indicator of climatic warming. Biol. Conserv. 56:63-78.
Briggs, SA, and Criswell, JH. 1979. Gradual silencing of spring in Washington. Atl. Nat.
32:19-26.
21
-------
Brittingham, MC, and Temple, SA. 1983. Have cowbirds caused forest songbirds to
decline? BioScience 33:31-35.
Butcher, GS, Niering, WA, and Barry, WJ, et al. 1981. Equilibrium biogeography and
the size of nature preserves: An avian case study. Oecologia 49:29-37.
Bystrak, D, and Robbins, CS. 1977. Bird population trends detected by the North
American Breeding Bird Survey. Polish Ecol. Studies 3:131-143.
Curtis, JT. 1956. The modification of mid-latitude grasslands and forests by man. In:
Man's role in changing the face of the earth, Chicago, IL: University of Chicago Press.
DellaSala, DA, and Rabe, DL. 1987. Response of least flycatchers, Empidonax minimus,
to forest disturbances. Biol. Conserv. 41:291-299.
Diamond, JM. 1984. "Normal" extinctions in isolated populations. In: Extinctions,
Chicago, EL: University of Chicago Press.
Faaborg, J, and Arendy, WJ. 1989. Long-term declines in winter resident warblers in a
Puerto Rican dry forest. Am. Birds 43:1226-1230.
Forman, RT, Galli, AE, and Leek, CF. 1976. Forest size and avian diversity in New
Jersey woodlots with some land use implications. Oecologia 26:1-8.
Galli, AE, Leek, CF, and Forman, RT. 1976. Avian distribution patterns in forest
islands of different sizes in central New Jersey. Auk 93:356-364.
Hall, GA. 1984. Population decline of neotropical migrants in an Appalachian forest.
Am. Birds 38:14-18.
Holmes, RT, Sherry, TW, and Sturges, FW. 1986. Bird community dynamics in a
temperate deciduous forest, long-term trends at Hubbard Brook. \ Epol. Monogr.
56:201-220. r ''
Holmes, RT, and Sherry, TW. 1988. Assessing population trends of New Hampshire
forest birds: Local vs. regional patterns. Auk 105:756-768.
Howe, RW. 1984. Local dynamics of bird assemblages in small forest habitat at islands
in Australia and North America. Ecology 65:1585-1601.
Hutto, RL. 1988. Is tropical deforestation responsible for the reported declines in
neotropical migrant populations? Am. Birds 42:375-379.
Jones, ET. 1986. The passerine decline. N. Am. Bird Bander 11:74-75.
22
-------
Kelly, ST, and DeCapita, ME. 1982. Cowbird control and its effect on Kirtland's
Warbler reproductive success. Wilson Bull. 94:363-365.
Leek, CF, Murray, BG, and Swinebroad, J. 1988. Long-term changes in the breeding
bird populations of a New Jersey forest. Biol. Conserv. 46:145-157.
Lovejoy, T. 1983. Tropical deforestation and North American migrant birds. Bird
Conserv. 1:126-128.
Lynch, JF, and Whigham, DF. 1984. Effects of forest fragmentation on breeding bird
communities in Maryland, USA. Biol. Conserv. 28:287-324.
Lynch, JF, and Whitcomb, RF. 1978. Effects of the insularization of the eastern
deciduous forest on avifaunal diversity and turnover. In: Marmelstein, A (ed.),
Classification, inventory, and evaluation of fish and wildlife habitat. Washington, DC:
US Fish and Wildlife Service. Publ. OBS-78176.
MacArthur, RH, and Wilson, EO. 1963. An equilibrium theory of insular biogeography.
Evolution 17:373-387.
MacArthur, RH, and Wilson, EO. 1967. The theory of island biogeography. Princeton,
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Marshall, JT. 19887 Birds lost from a giant Sequoia forest during fifty years. Condor
90:359-372.
Mayfield, HF. 1977a. Brown-headed cowbird: Agent of extermination. Am. Birds
31:107-113.
Mayfield, HF. 1977b. Brood parasitism: Reducing interactions between Kirtland's
warblers and brown-headed cowbirds. In: Endangered birds: Management techniques for
preserving threatened species, Madison, WI: University of Wisconsin Press.
Moore, NW, and Hooper, MD. 1975. On the number of bird species in British woods.
Biol. Conserv. 8:239-250.
Morse, DH. 1980. Population limitation: Breeding or wintering grounds? In: Migrant
birds in the Neotropics: Ecology, behavior, distribution and conservation, Washington, DC:
Smithsonian Institution Press.
Morton, ES, and Greenberg, R. 1989. The outlook for migratory songbirds: "Future
shock" for birders. Am. Birds 43:178-183.
23
-------
Payne, RB. 1977. The ecology of brood parasitism in birds. Ann. Rev. Ecol. Syst.
8:1-28.
Perez-Rivera, RA. 1986. Parasitism by the Shiny Cowbird in the interior parts of Puerto
Rico. J. Field Ornith. 57:99-104..
Rappole, JH, et al. 1983. Nearctic avion migrants in the neotropics. Washington, DC:
US Fish and Wildlife Service.
Robbins, CS. 1979. Effects of forest fragmentation on bird populations. In:
Management of north central and northeastern forests for nongame birds, St. Paul, MN:
North Central Forest Experiment Station.
Robbins, CS. 1980. Effects of forest fragmentation on breeding bird populations in the
Piedmont of the mid-Atlantic region. Atl. Nat. 33:31-36.
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Rothstein, SI, Verner, J, and Stevens, E. 1984. Radio tracking confirms a unique diurnal
pattern of spatial occurrence in the parasitic brown-headed cowbird. Ecology 65:77-88.
Serrao, J. 1983. 1983 Breeding Bird Census. Bull. Palisades Nat. Assoc.
Serrao, J. 1985. Decline of forest songbirds. Records of NJ Birds 11:5-9.
Sherry, TW and Holmes, RT. 1992 (in press). Population fluctuations in a long-distance
neotropical migrant: Demographic evidence for the importance of breeding season
events in the American redstart. In: Hagan and Johnston (eds.), Ecology and
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24
-------
Temple, SA, and Temple, BL. 1976. Avian population trends in central New York state,
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avifauna of forest fragments. Am. Birds 31:3-5.
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25
-------
Wiley, JW, Post, W, and Cruz, A. 1991. Conservation of the yellow-shouldered
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2.1.5. Popular Press Bibliography
Booth, W. 1989. Tropical forest loss may be killing off songbirds, study says.
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Brody, JE. 1989. Annual bird counts are starting to yield scientific insights. New York
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pp 26, 34, 48.
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1989, vol 138, col 1, pp B12, C5.
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Luoma, JR. 1988. Nation's suburbs blamed for songbird decline; also, efforts to aid
some wildlife are harming birds. New York Times. June 21, 1988, vol 137, col 5, p Cl.
Science News. 1991. Development makes songbirds easy prey. Science News 140 (Aug
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Stripp, D. 1991. You can't see the birds without the trees. Wall Street Journal.
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Wallace, J. 1986. Where have all the songbirds gone? Sierra (March/April):44-47.
Wilcove, DS, and Whitcomb, RF. 1983. Gone with the trees. Natural History.
26
-------
2.2. North American Freshwater Fish
Summary. The rate of extinctions of North American freshwater fish has risen
sharply in the last decade. Now, fully a third of the native species of North American
freshwater fish are considered threatened, endangered, or of special concern. Physical
alteration of surface waters (e.g., channelization, dams, reservoirs) and the introduction
of non-native species are the major causes of population declines and extinctions among
North American fish, although other factors have contributed to the decline of many
species. Native North American anadromous fish2 (e.g., salmon, steelhead) also are at
increasing risk of extinction, but we restrict our discussion here to fish that inhabit only
freshwater.
2.2.1. Description
Background. North America has a rich freshwater fish fauna, exhibiting the
greatest diversity in the central and southeastern United States (Exhibit 2.2.1). Many
fishes have limited ranges, particularly in the arid southwestern states and in Mexico.
Habitat characteristics that limit the distribution of species include water temperature,
water depth, flow rate, bottom type, presence and type of aquatic vegetation, turbidity,
and physical barriers between habitats.
Trends. The American Fisheries Society (AFS) Endangered Species Committee
(ESC) has identified documented extinctions of 40 taxa of freshwater fish (i.e., 3 genera,
27 species, and 13 subspecies) in North America in the past 100 years, half occurring
since 1965 (Miller et al., 1989) and 10 occurring in the last decade (Williams et al., 1989)
(Exhibits 2.2.2 and 2.2.3). The regions of North America that have lost "a substantial
proportion" of their native fish
fauna are the Great Lakes,
Great Basins, Parras Valley,
Valley of Mexico, the Rio
Grande, and other North
American southwest desert
areas (Miller et al., 1989). The
minnow family (Cyprinidae) has
lost more taxa (16) than any
other family of fishes, and
salmonids and cyprinodontids
have each lost 7 taxa (Miller et
al., 1989).
2Anadromous species inhabit both marine and freshwater ecosystems at different stages in their life-
histories. The adults live in the ocean, but ascend rivers for breeding. The juveniles then descend the
river to enter and mature in the ocean.
27
-------
Exhibit 2.2.1. Numbers of taxa of native freshwater fishes of selected river systems.
CLARK FORK
12
38
YELLOWSTONE
SACRAMENTO
34
SAN JOAQUIN
COLORADO
North America has a rich freshwater fish fauna, with the greatest diversity found in the central
and southeastern United States. Rivers selected to illustrate regional trends in fish species diversity.
Source: Reprinted from Sheldon (1988) with permission of Blackwell Scientific Publications.
28
-------
Exhibit 2.2.2. Cumulative number of fish extinctions by decade in the United States
during the past century.
40 -i
35 -
'o
o
v> 30
JQ
(n
-a
V)
o
'o
o
3
25 -
20-
15 -
0)
I 1°H
i
5 5H
13 species have
become extinct since
the Endangered
Species Act
was passed in 1966
1890 1900 1910 1920 1930 1940 1950 1960 1970 1980 1990
Year
The number of North American freshwater fish extinctions that occur each decade has been
increasing steadily since the turn of the century. In the United States alone, 32 species and
subspecies offish have become extinct since 1900, 13 since the Endangered Species Act was
passed in 1966.
Source: Based on 27 species extinctions plus 13 subspecies extinctions as described by Miller et al. (1989).
29
-------
Exhibit 2.2.4. AFS/ESC list of freshwater fish taxa in North America that are
endangered, threatened, or of special concern.
North American
Freshwater
Fish Families
Minnow
Perch
Killifish
Trout
Sucker
Bullhead Catfish
Sculpin
Sunfish
Sturgeon
Uvebearer
Gobie
Cavefish
Smelt
Lamprey
Stickleback
Silverside
Mudminnow
Paddlefish
Surfperch
Sleeper
r-
0
Endangered = 103 Taxa
Threatened = 114 Taxa
D Special Concern = 147 Taxa
10
—r~
20
~T—
30
40 50 60
Number of Species and Subspecies
70
80
Of approximately 1,000 species and subspecies of freshwater fish in North America, the
American Fisheries Society lists approximately 36 percent as endangered (i.e., facing extinction
in all or a significant portion of their range), threatened (i.e., likely to become endangered in
the near future), or of special concern (Le,, for which minor disturbances to their habitat could
place them in danger).
Source: Wffliams et al, 1989.
32
-------
Exhibit 2.2.5. Number of fish species endangered, threatened, or of special concern by
state.
Nevada
California
Tennessee
Alabama
Oregon
Texas
Arizona
North Carolina
Virginia
Georgia
New Mexico
Arkansas
Kentucky
Mississippi
Missouri
Illinois
Louisiana
Utah
Florida
Indiana
New York
Oklahoma
Colorado
Kansas
West Virginia
Ohio
Pennsylvania
South Carolina
Wisconsin
Wyoming
Iowa
Michigan
Minnesota
Montana
Nebraska
Idaho
North Dakota
South Dakota
Hawaii
Maryland
Washington
Maine
Connecticut
Delaware
Massachusetts
New Hampshire
New Jersey
Rhode Island
Vermont
Alaska
Special Concern
Threatened
Endangered
Number of Species
Source: Adapted from Williams et al., 1989.
33
-------
Exhibit 2.2.6. Proportion of freshwater fish species per 1,000 river miles classified by
AFS as endangered, threatened, or of special concern, by state.
Hawaii
Nevada
New Mexico
Delaware
Rhode Island
Tennessee
Arkansas
California
Arizona
Georgia
Kentucky
Utah
Illinois
Mississippi
South Carolina
Florida
Louisiana
Virginia
Alabama
Kansas
Missouri
North Carolina
Oklahoma
South Dakota
Indiana
North Dakota
Wyoming
Iowa
Vermont
West Virginia
New Jersey
Idaho
Texas
Colorado
Oregon
Nebraska
Massachusetts
Connecticut
Maryland
Michigan
Wisconsin
Ohio
Pennsylvania
New York
New Hampshire
Montana
Washington
Maine
Minnesota
Alaska
H11.5
5.7
5.7
Special Concern
Threatened
Endangered
0.5 1 1.5 2 2.5 3
Number of species per 1,000 river miles
3.5
Source: Adapted from Williams et al., 1989.
34
-------
Exhibit 2.2.7. Causes of extinctions and population declines in North American
freshwater fish.
% Contribution to if
Cause Species Extinctions3
Habitat destruction/modification
Introduced species
Hybridization
Pollution, chemical alteration
Overfishing
Disease
Acidification
73%
68%
38%
38%
15%
—
% Contribution to
Population Declines15
98%
up to
—
up to
3%
2% .
37%
37%,
increasing
Habitat destruction and modification is the leading cause of extinction and population declines
in North American freshwater fishes. Introduced species, hybridization, and pollution or
chemical alteration are the next most significant problems.
a Source: Miller et al., 1989
b Source: WUliams et al., 1989; Deacon et al. 1979
35
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2.23. Continued Monitoring
The AFS/ESC compiles a list of endangered, threatened, or species of special
concern in North America from other lists, original data, and discussions with pertinent
agencies and knowledgeable individuals. AFS/ESC has published three lists to date: in
1972, 1979, and 1989 (Miller, 1972; Deacon et al., 1979; Williams et al., 1989). The lists
are circulated to each state or provincial fish and game department for review and then
revised and published.
2.2.4. References
Deacon, JE, Kobetich, G, and Williams, JD, et al. 1979. Fishes of North America
endangered, threatened, or of special concern: 1979. Fisheries 4:29-44.
Hocutt, CH, et al. 1986. Zoogeography of the fishes of the central Appalachians and
central Atlantic coastal plain. In: The zoogeography of North American freshwater fishes,
New York, NY: John Wiley.
Kynard, BE. 1979. Population decline and change in frequencies of lateral plates in
threespine sticklebacks. Copeia 1979:635-638.
McAllister, DE, Parker, BJ, and McKee, PM. 1985. Rare, endangered and extinct fishes
in Canada. Natl. Mus. Canada. Natl. Mus. Nat. Sci. Syllogeus No. 54.
Meffe, GK, Hendrickson, DA, and Minckley, WL. 1983. Factors resulting in decline of
the endangered Sonoran topminnow Poeciliopsis occidentals (Atheriniformes: Poeciliidae)
in the United States. Biol. Conserv. 25:135-159.
Miller, RR. 1961. Man and the changing fish fauna of the American Southwest. Pap.
Mich. Acad. Sci. Arts Lett. 46:365-404.
Miller, RR. 1972. Threatened freshwater fishes of the United States. Trans. Am. Fish
Soc. 101:239-252.
Miller, RR, Williams, JD, and Williams, JE. 1989. Extinctions of North American fishes
during the past century. Fisheries 14:22-38.
)
Minckley, WL, and Deacon, JE. 1968. Southwestern fishes and the enigma of
'endangered species'. Science 159:1424-1432.
Mlot, C. 1989. Great Lakes fish and the greenhouse effect. BioSci. 39:145.
Moyle, PB. 1976a. Fish introductions in California: History and impact on native fishes.
Biol. Conserv. 9:101-118.
38
-------
Moyle, PB. 1976b. Inland fishes of California. Berkeley, CA: University of California
Press.
Ono, RD, Williams, JD, and Wagner, A. 1983. Vanishing Fishes of North America.
Washington, DC: Stone Wall Press.
Parker, BJ, and Brousseau, C. 1988. Status of the Aurora trout, Salvelinus fontinalis
timagamiensis, a distinct stock endemic to Canada. Can. Field-Nat. 102:87-91.
Schoenherr, AA. 1981. The role of competition in the replacement of native fishes by
introduced species. In: Fishes in North American deserts, New York, NY: John Wiley.
Sheldon, AL. 1988. Conservation of stream fishes: Patterns of diversity, rarity, and risk.
Conserv. Biol. 2:149-156.
Williams, JE, Johnson, JE, and Hendrickson, DA, et al. 1989. Fishes of North America,
endangered, threatened, or of special concern: 1989. Fisheries 14:2-20.
Williams, JE, and Miller, RR. 1990. Conservation status of the North American fish
fauna in fresh water. J. Fish Biol. 37 (Suppl. A):79-85.
Williams, JD, and Finnley, DK. 1977. Our vanishing fishes, can they be saved? Acad.
Nat. Sci. Phil. Frontiers 41:21-32.
Williams, JE, Bowman, DB, and Brooks, JE, et al. 1985. Endangered aquatic
ecosystems in North American deserts with a list of vanishing fishes of the region. J.
Arizona-Nevada Acad. Sci. 20:2-61.
Winston, MR, Taylor, CM, and Pigg, J. 1991. Upstream extirpation of four minnow
species due to damming of a prairie stream. Trans. Am. Fish. Soc. 120:98-105.
2.2.5. Popular Press Bibliography
Botkin, D. 1991. The tiny fish that may eat a water system: The debate over whether
to save the three-inch delta smelt highlights the narrow-mindedness of our environmental
laws (Sacramento River Delta). Los Angeles Times. June 16, 1991, vol 110, col 5, p Ml.
Gutis, PS. 1988. Unusual fish kill stirs new fears of decline in the region's waters. New
York Times. July 3, 1988, vol 137, col 1, section 1, pp 14, 1.
LAT. 1989. Pesticides cited in decline of fish. Los Angeles Times. December 20, 1989,
vol 109, col 3, p A28.
39
-------
National Wildlife. 1991. Aquatic life disappearing faster than land species. National
Wildlife 29:25.
NYT. 1990. From minnow to sturgeon, North American fish are in peril. New York
Times. January 30, 1990, p C4.
NYT. 1991. Deaths of fish spark dispute in Louisiana. New York Times. August 1
1991, p A12.
PRN. 1989. Spring fish kills reported. PR Newswire. May 5, 1989.
PRN. 1989. Update: Fish kills in Black and Chehalis Rivers. PR Newswire. August 17
1989.
PRN. 1990. Issaquah fish kill investigation continues. PR Newswire. May 16, 1990.
Reiger, G. 1991. The striper situation (decline of striped bass populations). Field and
Stream 95:13-15.
Williams, JD, and Finnley, DK. 1977. Our vanishing fishes: Can they be saved? Acad.
Nat. Sci. Phil. Frontiers 41:21-32.
40
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2.3. Ducks in North America
Summary. Numerous species of ducks have suffered significant declines in
population levels in North America in recent years (i.e., mallard, American wigeon, blue-
winged teal, northern pintail, and redhead), and several other species appear to be
declining also (e.g., canvasback, northern shoveler, green-winged teal). In the last 15
years, the overall breeding population of ducks has dropped by 24 percent. Investigators
believe that the declines are due primarily to drought and human activities that have
severely reduced the abundance of wetland habitats required by waterfowl for both
breeding and overwintering. Crowding of birds into the remaining areas may contribute
to outbreaks of disease and increased mortality. Degradation of the remaining wetlands
by acid rain and/or agricultural runoff may be reducing the reproductive success of ducks
in the remaining habitats. Uncovered oil pits contributed significantly to the mortality of
migratory waterfowl until recently, but uncovered cyanide ponds used by the gold mining
industry remain a threat.
2.3.1. Description
Background. About one half of North American duck populations breed in the
western prairie pothole regions of south-central Canada and the north-central United
States (Smith et al., 1964). In general, ducks prefer well-vegetated areas in close
proximity to open water for nesting sites (Bellrose, 1976). The aquatic invertebrates of
the potholes and other wetlands provide food for females during egg production and for
ducklings until fledging (Palmer, 1962).
Trends. The most recent US Fish
and Wildlife Service (FWS) May Breeding
Waterfowl and Habitat Survey indicates
that the 1991 spring breeding population
for ducks was 19 percent below the long-
term average from 1955-1990 (Exhibits
2.3.1 and 2.3.2). In the last 15 years, the
number of breeding ducks and geese
overall in North America has dropped
from 34 million to 26 million, a drop of 24
percent. Between 1985 and 1990 alone,
many waterfowl populations declined to
their lowest levels in three decades (data
in US FWS, 1991).
41
-------
(S3
C/9
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.g
1
I
.g
I
ns
oo
(SUOIIHUI) uoiieindod 6uipaajg >jona Buuds
I « 5
S S8 a
58 I ** £
^ 8 §
I?
f! I!
SJ «> ° -a
^£ -g|
I "^ ^•i
"I * I .a
•d s t« s
18 § S §
s s a §
^ *» »,V rt
His
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§• 8 £ *
S« § i .a
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I
-------
Exhibit 2.3.2. Changes in breeding population estimates for ten species of ducks in 1991
compared with 1955 to 1990.
Between
1990 and 1991
Between 1991
and the
1955-90 Average
Percent Change
Mallard
Gadwall
American wigeon
Green- winged teal
Blue-winged teal
Northern shoveler
Northern pintail
Redhead
Canvasback
Scaup
Total Dabblers & Divers**
+ 1
-3
+ 11
-9
+ 34
-3
-20
-6
-9
+ 25
+ 6
P Percent Change
0.430
0.382
0.183
0.188
<0.001
0.333
0.015
0.277
0.268
0.004
0.028
-27
+ 22
-14
-4
-10
-8
-62
-26
-16
-7
-19
P
<0.001
0.001
0.004
0.250
0.042
0.051
<0.001
<0.001
0.070
0.121
<0.001
Excludes scoters, eiders, oldsquaws and mergansers in strata 1-50.
Although there has been a slight increase in several duck populations in the last year (1990 to
1991, first two columns), overall, there has been a significant 19 percent decline in total
dabbler (e.g., mallard) and diving duck (e.g., scaup) breeding population levels as of 1991
compared with the previous 35 years (last two columns).
Source: Reproduced from US FWS (1991) with permission of the Director, US FWS.
43
-------
Exhibit 23.4. Summary of the number of May ponds (adjusted for visibility) in portions
of Prairie Canada and the northcentral United States, 1990 and 1991.
-67
-46
-f-
Total Northern U.S. Prairie
South Dakota
North Dakota
1 Montana
Total Southern Canadian Prairie
Southern Manatoba
Southern Saskatchewan
1 Southern Alberta
1
-70 -60 -50 -40 -30 -20 -10 0 10
Percent Change from the Long-term Average in the Number of Ponds Counted in May, 1990 and May, 1991
Long-term trend for Canadian prairie is measured from 1961 to 1990
Long-term trend for U.S. prairie is measured from 1974 to 1990
Canada, which provides the majority of wetlands used by breeding waterfowl in North America,
has suffered a 29 percent loss of wetlands compared with the past 30 years. The United
States, with a smaller portion of the waterfowl breeding habitat, has suffered a 41 percent loss,
compared with the past 16 years.
Source: Reproduced from US FWS (1991) with permission of the Director, US FWS.
46
-------
contributed to a loss of wetland habitat, particularly over the last decade. Each of these
is discussed briefly below.
Land development. Wetland breeding habitats have been severely
impacted by human activities; filling and development of wetland areas and
diversions of water for agriculture, industry, and domestic uses have contributed to
loss of wetlands. Agriculture alone accounted for 87 percent of the wetland
conversions between 1954 and 1974 (US FWS, 1990). The US FWS estimates
that 53 percent of the wetlands existing in the conterminous United States as of
the 1780's were lost by 1980 (Dahl, 1990). Terborgh (1989) estimated that
waterfowl breeding habitat has declined by 80% to 90% from presettlement times.
Much of the wetland losses have occurred recently. For example, about 50% of
the coastal wetlands on the Atlantic Flyway have been destroyed since 1953 (Jerry
Serie of the US FWS as reported by Steinhart, 1989*P). Intensive agricultural
practices also have reduced nesting cover throughout the prairies (Reynolds et al.,
1990), which leads to increased nest predation and reduced reproductive success
(Sheehan et al., 1987). Wintering habitat also has been severely impacted. Half
of the waterfowl that migrate via the Pacific flyway overwinter in California's
Central Valley. The Valley originally contained 4,000,000 acres of wetlands, but
owing to agricultural and urban development, today only 280,000 acres remain, of
which only 100,000 are protected in State and Federal wildlife refuges (Steinhart,
1989*P).
Drought. Reduced rainfall in North America during the 1980's caused the
reduction of natural water sources and led to the diversion and use of the
remaining water for agriculture. Steinhart (1989*P) reported that 40 percent of
the prairie potholes disappeared between 1980 and 1988 primarily because of
drought. Drought also contributes to the destruction of essential nesting cover
(Reynolds et al., 1990). The US FWS identified drought as a principal factor
accounting for the sharp decline of duck populations in early 1960's and again in
the 1980's (Exhibit 2.3.1).
Acid deposition. There are two primary processes by which acid deposition
adversely affects waterfowl: (1) mobilization of metals that can bioaccumulate to toxic
levels in aquatic food chains^ and (2) changes in species composition in the food web.
Acid conditions tend to increase the solubility and mobility of metals which
bioaccumulate (e.g., cadmium) and other toxic metals (e.g., aluminum, lead) which can
lead to the disappearance of susceptible fish and invertebrate species (e.g., aquatic
insects, snails) on which the waterfowl depend for food (Diamond, 1989; Mitchell, 1989;
Schindler, 1988). Some studies have documented a reduction in egg-shell thickness
5Biomagnification occurs when a substance is found in higher concentrations at each higher level of
the food chain. The top predators accumulate the substance from their food, which consists of animals
that have accumulated the substance in their food.
47
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associated with acidic conditions (Diamond, 1989; Ormerod et al, 1988 as cited in
Mitchell, 1989). Data are not available to quantify the contribution of acid deposition
relative to other factors that contribute to declining waterfowl populations, however.
Agricultural runoff. Pesticides and other toxic substances, excessive nutrients, and
soil runoff from agricultural areas contaminate and alter many of the remaining wetland
waterfowl breeding grounds in North America. For example, severe reproductive
impacts occurred in ducks (e.g., mallard, northern pintail, cinnamon teal) nesting on
selenium-contaminated irrigation drainwater ponds in the Kesterson Refuge and around
the Kesterson reservoir in California in the mid 1980s (Ohlendorf et al., 1986, 1987).
Synthetic pyrethroid pesticide runoff into the prairie potholes of Canada is eliminating
the aquatic arthropod (i.e., insects and Crustacea) prey of the waterfowl nesting in the
potholes, resulting in reduced reproductive success in those areas (Sheehan et al., 1987).
Again, data are not available to quantify the contribution of agricultural runoff to
declining duck populations.
Disease. Bellrose (1976) and Stout and Cornwell (1976) have suggested that most
non-hunting mortality of ducks in recent years is the result of disease (e.g., avian cholera,
botulism). Dramatic outbreaks of avian botulism (Clostridiwn botulinum type C) in
western North America have killed tens of thousands of waterfowl, shorebirds, and other
aquatic birds in a few months (Enright, 1971; Hunter, 1970; Malcolm, 1982; National
Wildlife Health Center (NWHC) unpublished data as cited by Brand et al., 1988; Parrish
and Hunter, 1969) and have occurred at intervals since before the turn of the century
(Kalmbach and Gunderson, 1934). Outbreaks of avian botulism in the coastal region of
New York and New Jersey have been reported since 1950, with losses of several hundred
birds (Reilly and Boroff, 1967; Figley and Van Druff, 1982; as cited in Brand et al.,
1988). In the western states, the extreme crowding of waterfowl in remaining wetland
areas during the drought of the 1980's contributed to an increase in the incidence of
disease epidemics, notably avian cholera and botulism (Parrish and Hunter, 1969; Smith
and Higgins, 1990). For example, 20,000 birds died of botulism at the Stillwater Refuge
in Nevada in 1989 apparently as a consequence of overcrowding caused by low water
conditions (as reported by Moser, 1989*P). Smith and Higgins (1990) found an inverse
relationship between the density of remaining semipermanent wetland basins in Nebraska
and the frequency of avian cholera epidemics. This problem may be considered
secondary to the loss of breeding and wintering habitat, however.
Waste pits. In 1989, Federal wildlife officials estimated that pits and ponds used
"for storing oily industrial wastes were responsible for killing 500,000 migratory waterfowl,
including some 100,000 ducks, in parts of New Mexico, Texas, Oklahoma, Kansas and
Colorado in 1989 alone (Kelly, 1990*P; Bryce, 1991*P). Flying birds apparently are
attracted to uncovered oil pits, mistaking the reflections as a sign of fresh water. This
problem has been greatly reduced in recent years, however. In 1989, New Mexico passed
a law requiring that open oil pits and tanks be covered with netting. Texas passed a
similar law in 1991 (Bryce, 1991*P). Also in 1989, the US FWS escalated enforcement of
48
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the Federal Migratory Bird Treaty Act (MBTA) and has been prosecuting companies
that have not covered their pits. Cyanide leaching ponds, common in gold and other
mineral mining areas of the mid west, also kill waterfowl. The total number of birds
killed is unknonw, but a single pond was found to have killed 1,450 birds (including
ducks) over one eight month period (Bryce, 1991*P). The US FWS is continuing to
investigate this problem, but has limited law enforcement staff to cover the large areas of
concern.
2.3.3. Continued Monitoring
Each year since 1955, the US FWS has conducted a survey to estimate the
number and species of potential breeding ducks in the pertinent nesting areas of North
America. The survey, which begins in early May and continues until mid June, is
conducted via air, ground, and water by Federal, State, and Provincial (Canada)
personnel (Reynolds et al., 1990). The survey covers over 90 percent of the principal
waterfowl breeding areas in both the United States and Canada. The results of this
survey are reported annually.
There are other surveys that include data related to waterfowl population trends.
The US FWS conducts a duck production survey in July of each year, and provides an
index to the number, age, and size of broods produced and the number of adult birds still
on nesting territories. The US FWS Patuxent National Wildlife Research Center keeps
banding records that are used to estimate annual mortality rates of waterfowl
populations. For mallards, the annual production rate index, along with breeding
population and breeding season survival information, is used to predict a fall flight index
for this species (Reynolds et al., 1990).
The Canadian Wildlife Service also conducts surveys of waterfowl populations and
coordinates some of these with the US FWS.
Note about the 1991 US FWS Survey. The 1991 US FWS breeding duck population
estimates differ from previous years due to several improvements. Most importantly, the
information used to estimate the Visibility Correction Factor (VCF), which is necessary
when too few ducks are seen in an area to make a population estimate, has been
changed from the average of prairie VCFs from 1961-73 to include only the current and
prior years' data. This has resulted in a reduction of many of the historical population
estimates upon recalculation, because prairie averages were not appropriate for all
habitats and visibility has changed in recent years due to drought and intensive
agricultural practices. Exhibit 2.3.5 shows how historical mallard population estimates
have changed as a result of the new VCF estimation method. Also this year's Survey has
been expanded to include additional transects in traditional survey areas, and there are
plans to initiate activities in areas not currently included in the May Breeding Waterfowl
Survey (US FWS, 1991).
49
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Exhibit 23.5. US FWS May Breeding Waterfowl Survey estimates for mallards from
1955 to 1991 using old and new estimation methods.
14H
12-
10-
•M
ESS
8-
6-
55
58
61
64
67
70
73
Year
76
79
82
85
88 91
Solid line represents estimates based on new analytical procedures with 95% statistical
confidence intervals. Dashed line represents estimates based on the old estimation procedures.
Source: Reproduced from US FWS (1991) with permission of the Director, US FWS.
50
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2.3.4. References
Bellrose, FC. 1976. Ducks geese and swans of North America. Harrisburg, PA: Stackpole
Books.
Blancher, PJ, and McAuley, DG. 1987. Influence of wetland acidity on avian breeding
success. Trans. N. Am. Wildl. Nat. Res. Conf. 52:628-635.
Bolen, EG. 1982. Playa wetlands of the US Southern High Plains: Their wildlife values
and challenges for management. In: Gopal, B, Turner, RE, and Wetzel, RG, et al.,
(eds.), Proceedings First International Wetlands Conference, Jaipur, India: National Inst.
Ecology and International Scientific Publications. Pp. 9-20.
Brand, CJ, Windingstad, RM, and Siegfried, LM, et al. 1988. Avian morbidity and
mortality from botulism Aspergillosis and Salmonellosis at Jamaica Bay Wildlife Refuge
New York, USA. Colonial Waterbirds 11:284-292.
Dahl, TE. 1990. Wetland losses in the United States 1780's to 1980's. Washington, DC:
US Department of the Interior, Fish and Wildlife Service.
Diamond, AW. 1989. Impacts of acid rain on aquatic birds. Environ. Monitor. Assess.
12:245-254.
Enright, CA. 1971. A review of research on type C botulism among waterbirds. Fort
Collins, CO: Colorado Cooperative Wildlife Research Unit, Colorado State University.
Fedynich, AM, and Godfrey, RD Jr. 1988. Waterfowl mortality surveys on the southern
high plains of Texas USA. Southwest Nat. 33:185-192.
Figley, WK, and VanDruff, LW. 1982. The ecology of urban mallards. Wildl. Mono.
81:1-40.
Hunter, BF. 1970. Waterfowl botulism in California ~ 1969. Calif. Fish Game
56:207-208.
Kalmbach, ER, and Gunderson, MF. 1934. Western duck sickness, a form of botulism.
Washington, DC: US Department of Agriculture. US Department of Interior Tech.
Bull. No. 41.
Malcolm, JM. 1982. Bird collisions with a power transmission line and their relation to
botulism on a Montana wetland. Wildl. Soc. Bull. 10:297-304.
51
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Mitchell, BA. 1989. Acid rain and birds: How much proof is needed? Am. Birds
43:234-241.
Ohlendorf, HM, Hoffman, DJ, and Saiki, MK, et al. 1986. Embryonic mortality and
abnormalities of aquatic birds: Apparent impacts of selenium from irrigation drainwater.
Sci. Total Environ. 52:49-63.
Ohlendorf, HM, Hothem, RH, and Aldrich, TW, et al. 1987. Selenium contamination of
The Grasslands, a major California waterfowl area. Sci. Total Environ. 66:169-183.
Ormerod, SJ, Bull, KR, and Cummins, CP, et al. 1988. Egg mass and shell thickness in
Dippers Cinclus cinclus in relation to stream acidity in Wales and Scotland. Environ.
Poll. 55:107-121.
Palmer, RS. 1962. Handbook of North American birds. New Haven, CT: Yale
University Press.
Parrish, JM, and Hunter, BF. 1969. Waterfowl botulism in the Southern San Joaquin
Valley, 1967-68. Calif. Fish Game 55:265-272.
Pence, DB. 1981. The effects of modification and environmental contamination of playa
lakes on wildlife morbidity and mortality. In: Barclay, JS, and White, WV, (eds.),
Proceedings Playa Lakes Symposium. Washington, DC: Office Biol. Serv., US
Department of the Interior Fish and Wildlife Service. Pp. 83-93.
Reilly, JR, and Boroff, DA. 1967. Botulism in a tidal estuary in New Jersey. Bull.
Wildl. Disease Assoc. 3:26-29.
Reynolds, RE, Blohm, RJ, and Johnson, FA, et al. 1990. 1990 Status of waterfowl and
fall flight forecast. Canadian Wildlife Service and US Fish and Wildlife Service. July 25.
Schindler, DW. 1988. Effects of acid rain on freshwater ecosystems. Science
239:149-157.
Sheehan, PJ, Baril, A, and Mineau, P, et al. 1987. The impact of pesticides on the
ecology of prairie nesting ducks. Ottawa, Canada: Canadian Wildlife Service. Tech.
Rep. Ser. No. 19.
Smith, AG, Stoudt, JH, and Gollop, JB. 1964. Prairie potholes and marshes. In:
Linduska, JP (ed.), Waterfowl tomorrow. Washington, DC: US Fish and Wildlife
Service.
Smith, BJ, and Higgins, KF. 1990. Avian cholera and temporal changes in wetland
numbers and densities in Nebraska's USA rain water basin area. Wetlands 10:1-6.
52
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Stout, IJ, and Cornwall, GW. 1976. Nonhunting mortality of fledged North American
waterfowl. J. Wildl. Manage. 40:681-693.
Terborgh, J. 1989. Where have all the birds gone?, Princeton, NJ: Princeton University
Press.
US FWS. 1990. Wetlands: Meeting the president's challenge (1990 wetlands action
plan). Washington, DC: US Fish and Wildlife Service.
US FWS. 1991. Trends in duck breeding populations, 1955-91. US Fish and Wildlife
Service, Office of Migratory Bird Management: Laurel, MD. Administrative Report -
July 2, 1991.
WMI. 1989. Duck populations continue to plummet. Wildlife Management Institute
Outdoor News Bull. 43:1-2.
23.5. Popular Press Bibliography
Bryce, R. 1991. Caustic pits: The silent killer. Field & Stream 96: 54-55.
Faber, H. 1988. Duck conservation plan limits hunting season. New York Times.
October 9, 1988, vol 138, col 3, pp 36(N), 62(L).
Hodgson, M. 1991. Waterfowl 'rest stop' endangered; California's dwindling wetland
areas struggle against water shortages and urban creep. Christian Science Monitor.
January 10, 1991, edition All, section 'Habitat,' p. 12.
Irion, R. 1988. Drought helps two endangered species rebound, but it's a dismal year
for ducks. Washington Post. August 1, 1988, vol 111, col 1, p A14.
Kelly, S. 1990. Waste oil pits may have killed 500,000 birds in '89 - total in 5 states
exceeds losses in Exxon Valdez Spill. Washington Post. April 6, 1990, p A17.
Lancaster, J. 1990. Buying peace in western water war. Washington Post. June 19,
1990.
Moser, PW. 1989. A climate for death, (the past years drought and extreme weather
conditions took its toll on wildlife). Sports Illustrated 70:48.
NYT. 1988. Drought threatens duck species as their nesting areas dry up. New York
Times. June 28, 1988, vol 113, col 1, pp 24, C4.
53
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Pearce, M. 1988. Ducks done in by drought, agriculture. Wall Street Journal. October
17, 1988, col 1, pp A12, A20.
Pearce, M. 1990. Dark days for ducks. Wall Street Journal. March 28, 1990, col 1, p.
A12(W)(E).
Peterson, C. 1989. Toxic time bomb ticks in San Joaquin Valley; farm evaporation
ponds killing waterfowl. Washington Post. March 19, 1989, vol 112, col 1, p. A3.
PRN. 1988. Drought of 1988 causing big decline in duck populations; bad news for
hunters and related economies. PR Newswire. August 11, 1988.
Steinhart, P. 1989. Portrait of a deepening crisis. Natl. Wildl. (6):4-13.
Steinhart, P. 1990. Innocent victims of a toxic world. Eighteen years after DDT was
banned, America's wildlife suffers worse than ever from chemical pollution. National
Wildlife (2):20-27.
Toth, S. 1974. Botulism (western duck sickness) and its effects on waterfowl in New
Jersey. New Jersey Outdoors 1:12-14.
Williamson, LL. 1989. Duck populations continue to plummet. Outdoor News Bulletin
43:1-2.
54
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2.4. Coral Reef Communities Worldwide
Summary. For years, coral reef communities6 have been suffering from adverse
effects of human activities, including physical destruction (e.g., boat anchors, coral
mining), nutrient runoff and sedimentation, and coastal pollution from agriculture,
industries, and sewage. In addition, during the 1980's, four coral reef community
bleaching events occurred on an unprecedented geographic scale. While corals often
survive bleaching, they can be weakened and become more susceptible to other causes of
mortality. In some areas, the Galapagos for example, the reefs died almost a decade
ago, and have not yet recolonized.
Some scientists believe that these large-scale bleaching events occurred in
response to elevated water temperatures that might be associated with a global warming
trend added to other sources of coral reef community damages. Participants in a recent
National Science Foundation (NSF)-sponsored meeting (June, 1991), however, concluded
that there is no proof as yet of a global warming trend. Instead, the participants
concluded that wide-spread coral bleaching may represent the cumulative effect of local
perturbations that result from population growth, land use, and resource exploitation
(D'Elia et al., 1991). All scientists agree, however, that coral reef communities are
deteriorating at an unprecedented rate and scale. John Ogden, director of the Florida
Institute of Oceanography, has concluded
that "virtually every reef system in the
world is suffering" (NYT, 1990*P), and
Williams and Bunkley-Williams (1990a)
are concerned that the coral bleaching
cycles will continue, possibly with more
intensity, until "coral dominated reefs no
longer exist."
The coral reef bleaching events are
only one manifestation of major tropical
marine disturbances that appear to be
increasing in frequency. In 1990
(Williams, 1991) and again in March and
April of 1991 (Booth, 1991*P), a massive
die-off of black sea urchins occurred in
the Caribbean Sea and the Florida Keys.
This is the third massive die-off of this
group in this area since 1984; diademid
urchin populations first crashed in the
Caribbean Sea and western North Atlantic
"Drawing of coral reef in the box is reproduced with permission of the artist, Jo Moore.
55
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in 1983 and 1984, when 95 to 99 percent of the urchins in all locations declined
(Carpenter, 1990; Williams and Bunkley-Williams, 1990a). A massive die-off of diademid
urchins occurred in Hawaii in 1981. Other marine disturbances that may be related to
those of coral reef communities have included giant clam die-offs, turtle tumor outbreaks,
and recurring herring mortalities (Alder and Braley, 1989; Williams and Bunkley-
Williams, 1990b). In the remainder of this section, however, we focus on the coral reefs
and stony coral organisms which are responsible for building and maintaining the physical
structure of the reef.
2.4.1. Description
Background. Stony corals are coelenterates that produce a calcium carbonate
skeleton. Reef-building species of stony coral need relatively shallow water because of
the light requirements of the symbiotic zooxanthellae (dinoflagellate algae) that live in
their tissues (Barnes, 1968). These algae utilize wastes from the corals, supply up to 63
percent of the corals' nutrients, and facilitate calcification (Glynn, 1991). Without these
services, the stony corals cannot build their skeletons. The coral skeletons provide a
substrate for many other species. Tropical reefs are associations of usually several
thousand species of different animals, including fish, sea urchins, clams, Crustacea, and
many other groups of organisms. Other reef community members, including fire corals,
sea anemones, sponges, gorgonians, sea fans, soft corals, and giant clams, also use
photosynthetic symbionts.
Coral bleaching occurs when the corals lose or expel a majority of their
zooxanthellae, when the concentration of pigments in the zooxanthellae declines
markedly, or when some combination of these events occurs (Glynn, 1991). As a result,
the coral host becomes pale or "bleached" in appearance due to the loss of plant
pigments and the increased visibility of the coral's calcareous skeleton (Glynn, 1991).
Bleaching also can occur in the other photosymbiotic species (e.g., sea fans, soft corals).
Bleached corals may survive for some time without the nutrition supplied by the
zooxanthellae by consuming their own tissues, which can leave them unable to reproduce
(Szmant and Gassman, 1990). The extent of bleaching and tissue damage that can be
tolerated is unknown (Glynn, 1991).
The effects of bleaching events range from slight, with full recovery possible, to
severe, with most of the coral dying, and the skeletal remains eroding before new
recruitment from other areas is possible (Hayes and Bush, 1990; Holthus et al., 1989;
Glynn, 1991). In one study, continued bleaching was documented for more than a year
after the initial event (Bunkely-Williams et al., 1991). Recovering corals grow more
slowly than unbleached corals (Goreau and MacFarlane, 1990) and may not reproduce
(Szmant and Gassman, 1990). More than two to four years is required for a reef to fully
recover from an extensive bleaching event (Glynn and D'Croz, 1990; Suharsono, 1988).
56
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Trends. Coral reefs around the world have been declining and suffering damage
over the past 10 to 20 years (Williams and Bunkley-Williams, 1990a; D'Elia et aL, 1991).
Coral reefs are deteriorating in the Pacific (Gomez, 1988) and the Atlantic (Rogers,
1985; Lang as reported in Rollings, 1987*P) due to physical destruction (e.g., boat
anchors, coral harvesting), nutrient runoff and sedimentation, industrial or agricultural
chemicals, and sewage pollution. The affected areas include the coasts of Australia,
China, Japan, Panama, Thailand, Malaysia, the Philippines, India, Indonesia, Kenya, the
Red Sea, Colombia, the Caribbean, and the United States (NYT, 1990*P). In the
Florida Keys, corals are dying at a faster rate than 5 years ago, and some scientists
predict that the Florida reef may be dead by the year 2000 (J. Porter as reported by
Keating, 1991).
Until recently, isolated instances of coral bleaching have occurred in response to
heavy rains, pollutants, decreased salinity, or other local stresses (Roberts, 1987, 1988).
Worldwide coral bleaching events, or "complexes,"7 occurred in 1979/80, 1982/83,
1986/88, and 1989/90 (Glynn, 1991; Williams and Bunkley-Williams, 1990a). In 1980,
three widely separated areas in the Pacific suffered extensive bleaching: Australia
(Oliver, 1985), Easter Island (Cea-Egana and DiSalvo, 1982), and Okinawa (Yamazato,
1981). Bleaching also occurred in Florida in 1980 and in Bonaire in 1979 (Williams and
Bunkley-Williams, 1990a). In 1983, some coral species appear to have been eliminated
from the eastern Pacific (Glynn, 1984; Glynn and Weerdt, 1991), and 97 percent of the
corals on some reefs in the Galapagos Islands and other corals in the eastern Pacific
were killed (Glynn, 1991). The Great Barrier Reef of Australia bleached extensively in
1982, one year before the 1983 reports of bleaching in other areas (Williams and
Bunkley-Williams, 1990a). In the 1986/88 event, the areas most severely affected were
Florida, the Bahamas, and the Greater Antilles, while reefs off Bermuda, Curacao,
Lesser Antilles, Panama, Venezuela, and Tobago suffered less (Williams and Bunkley-
Williams, 1990a). The eastern Pacific bleached less in 1986/88 than in 1982/83; however,
overall, more bleaching occurred in more areas in 1986/87 than in 1982/83. For example,
the area bleached in Australia's Great Barrier Reef in 1987 was two to four times the
size of areas bleached there in 1982/83 (Williams and Bunkley-Williams, 1990a).
Williams and Bunkley-Williams (1990b) received numerous reports of coral
bleaching events in mid-to-late 1989 from many areas of the Caribbean and predicted
that a larger scale bleaching event would occur in 1990. The most severe and extensive
coral reef bleaching event ever reported occurred in the tropical western Atlantic in 1990
(Williams, 1991). Mass mortalities of fire coral and some stony corals occurred in the
beginning of the event. The most severe bleaching seemed to occur in the Northern
Caribbean, Bahamas, Florida, Texas, and Bermuda, but some severe-to-moderate
bleaching appears also to have occurred throughout much of the Caribbean and in
Hawaii, Australia, and Fiji. Bleaching in French Polynesia was reported in June, 1991
7Groups of time-related bleaching events.
57
-------
(Williams and Grizzle, 1991). Exhibits 2.4.1 to 2.4.4 show the worldwide distribution of
these bleaching events.
Some corals have recovered from the bleaching events described above whereas
others have not. Coral cover on an Indonesian reef attained 50 percent of its former
level after five years (Brown and Suharsono, 1990; as cited in Glynn, 1991). On the
other hand, on eastern Pacific coral reefs that suffered high coral mortality in 1982/83,
bioerosion now exceeds net carbonate production, which threatens to reduce the reef
skeleton to sediment (Glynn, 1988). In the Galapagos Islands, no recruitment of reef
building organisms has been observed after seven years (Glynn, 1988). Similarly, some
reefs along the Pacific coast of Costa Rica exhibited 100% mortality in 1982/83 and
recruitment has been minimal since, prompting experiments in restoration by
transplanting living coral fragments from elsewhere onto the dead reef framework
(Guzman, 1991).
2.4.2. Hypotheses
Many of the physical causes of coral reef community deterioration are
incontrovertible (e.g., physical destruction, nutrient runoff and sedimentation, point
source pollution) and also may contribute to the observed incidence of disease. There
are natural causes (e.g., hurricanes) that physically stress the reefs as well. The general
scientific consensus is that bleaching (i.e., expulsion of zooxanthellae) is stress-induced.
Elevated water temperature has been accepted by many as the primary cause of the
large-scale bleaching events (D'Elia et al., 1991; Goreau et al., 1991; Williams and
Bunkley-Williams, 1990a). Coral stress induced by pollution, sedimentation, and physical
destruction may prevent corals from withstanding temperature changes that normally
would have little effect (Bunkley-Williams and Williams, 1990). Each of these hypotheses
is discussed below.
Physical destruction. On certain coral reefs, the number of visitors and boats has
increased dramatically in the last 30 years, and direct coral harvesting and damage from
boats appears to be increasing (Ward, 1990*P). Years ago, Davis (1977) found that 20
percent of the staghorn corals in Fort Jefferson National Monument, Dry Tortugas,
Florida, showed severe damage from anchors. Dustan and Halas (1987) found continued
degradation of a Florida coral reef from 1975 to 1983 due to physical disturbances in the
shallow areas. Some investigators have argued that predation on scleractinian corals of
the western Pacific by the crown-of-thorns starfish (Acanthaster planet) which physically
removes large sections of reef, is attributable to human disturbances of natural predators
on the starfish, although there is some debate over this hypothesis (Walbran et al., 1989).
Nutrient runoff and sedimentation. Freshwater runoff, with associated sediment
loads, can have adverse effects on coral communities. Runoff usually is loaded with both
sediments and nutrients. Dustan and Halas (1987) and Acevedo and Goenaga (1986)
have documented examples of deterioration of reefs off Florida and Puerto Rico due to
58
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deposition of nutrient-laden sediments. Prime coral reef habitat is a low-nutrient
environment. The nutrients may allow algae to grow quickly and to smother the corals,
blocking light and trapping sediment (Pastorok and Bilyard, 1985). Off the Florida Keys,
the most important threat to the reefs appears to be excessive nutrient loading from
agricultural fertilizers and septic tanks, which has caused increased algal growth on the
corals (Keating, 1991*P; Lauter, 1991*P). Lapointe (1989*P) believes that algal reefs
will replace coral reefs in the Caribbean as a direct result of nutrification. Sediments in
runoff also can smother reefs, reducing the number of species present and the percent
cover, as shown in Exhibit 2.4.5 (Pastorok and Bilyard, 1985). Excess sedimentation
results from land clearing, road building, and river and stream channelization. In some
areas, increased runoff of nutrients and sediments as a consequence of rainforest
destruction has caused deterioration of coral reefs (Glynn, 1991).
Point source pollution. Coastal sewage discharges and oil spills have contributed to
local declines of coral reefs. The three components of sewage pollution that are most
detrimental to corals are nutrients and sediments, as discussed above, and toxic
substances (e.g., PCBs, metals, chlorine, pesticides, and petroleum hydrocarbons).
Sewage is threatening the coral reef communities of the Red Sea, Caribbean, Hawaii,
and the Caroline Islands (Pastorok and Bilyard, 1985). Oil spills also are damaging coral
reef communities. In 1986, more than eight million liters of crude oil spilled into the sea
on the Caribbean coast of Panama. Among other adverse effects on the reefs, there was
extensive mortality of shallow subtidal corals; at depths less than three meters, the
abundance of the most common scleractinian coral decreased by 51 percent to 96
percent, and total coral cover decreased by 75 percent (Jackson et al., 1989). Algae
invaded the reef, and formed dense mats. Three years after the spill, oil continued to
ooze out of the mangrove sediments onshore and the corals had not fully recovered
(Booth, 1989*P).
Disease. Increased incidence of disease (e.g., black band disease, white band
disease) has been associated with increased physical damage, pollution, and
sedimentation of corals (Bunkley-Williams and Williams, 1990; Dustan and Halas, 1987),
but firm evidence for cause and effect is lacking. Dustan and Halas (1987) point out that
the observed diseases occur naturally, but poor water quality may contribute to their
spread and severity.
Natural phenomena. Hurricanes can fragment coral reefs, and thereby weaken
them (Bunkley-Williams and Williams, 1990; Dustan and Halas, 1987; Woodley et al.
1981). Extreme low tides associated with El Nifios - Southern Oscillations (ENSO)
events8 have been known to leave coral reefs exposed, which can contribute to coral
bleaching and death (Bunkley-Williams and Williams, 1990; Yamaguchi, 1975; Glynn,
8ENSOs are periodic worldwide meteorological shifts associated with changes in ocean currents and
atmospheric circulation lasting several months to two years.
63
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Exhibit 2.4.5. Pnral
a global wanning trend, the corals may have only recently been exposed to temperatures
that exceed their tolerance levels (Exhibit 2.4.6a). Second, cumulative effects from
human perturbations (e.g., physical destruction, nutrient runoff and sedimentation, and
other pollution) may be weakening the corals, reducing their tolerance of high
temperatures (Exhibit 2.4.6b). Finally, both processes could be occurring.
Obtaining accurate data on global ocean temperatures is difficult (Bunkley-
Williams and Williams, 1990; Glynn, 1991). The extreme temperatures of the last decade
have most likely caused temperatures that the corals could not tolerate (D'Elia et al.,
1991; Goreau et al., 1991; Williams and Buiikley-Williams, 1990a), but the hypothesis that
this reflects widespread ocean warming as a consequence of global warming has not been
substantiated (Glynn, 1991; D'Elia et al., 1991). The consensus of a National Science
Foundation (NSF)-sponsored meeting on the issue in June, 1991, was that there is no
proof that global warming is already happening, and therefore, it is not possible to claim
that coral bleaching is an early indicator of the phenomenon (D'Elia et al., 1991). The
group agreed, however, that reef deterioration world-wide is a serious problem.
2.43. Continued Monitoring
The Marine Ecological Disturbance Information Center (MEDIC), maintained at
the Department of Marine Sciences at the University of Puerto Rico (P.O. Box 908,
Lajas, PR 00667), is serving as a communication hub for information concerning not only
coral reef bleaching events, but other major marine disturbances including sea urchin
mass mortalities, fish Mils, and turtle tumor outbreaks. Dr. Ernest Williams serves as the
Caribbean Coordinator at the University of Puerto Rico and Dr. John Grizzle serves as
the Auburn University Coordinator. MEDIC publishes a newsletter at regular intervals
summarizing recent reports of marine disturbances and efforts are underway or planned
to further study the phenomena and their implications.
The participants in the NSF-sponsored meeting in June, 1991, unanimously
recommended an international program of intensive, long-term monitoring of coral reef
communities throughout the world to collect data on the physical and biological factors
that can affect reef health. Their recommendations will go to NSF, the National
Oceanographic and Atmospheric Administration (NOAA), and EPA (D'Elia et al., 1991).
2.4.4. References
Acevedo, R, and Goenaga, C. 1986. Note on a coral bleaching after a chronic flooding
in southwestern Puerto Rico. Carib. J. Sci. 22:225.
Alder, J, and Braley R. 1989. Serious mortality in populations of giant clams on reefs
surrounding Lizard Island, Great Barrier Reef, Australia. Aust. J. Marine Freshwater
Res. 40:205-214.
66
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Exhibit 2.4.6. Model of causes of worldwide coral reef bleaching.
CD
Q.
(a)
Bleaching Events
Yearly Seasonal
Temperature Increase
Coral Temperature
Tolerance
Warming Trend ?
(b)
Yearly Seasonal
Temperature Increase
Bleaching Events
Declining Tolerance to
Warm Temperatures
Time in Years
The model of causes of worldwide coral reef bleaching consists of several components. Elevated
temperatures occur each year during the summer. During an ENSO or other temporary
warming event, high temperatures sufficient to bleach hosts can occur. Up to three seasonal
peaks of temperature can be superimposed on a single ENSO or other warming event. The
middle event (i.e., main event) produces the more severe bleaching and mortalities because it
occurs at the height of the temporary ENSO or other warming event. The preceding and
following events are less severe because they are on the 'shoulders' of the temporary warming
event.
(a) If a general warming trend were occurring in the oceans, the frequency and severity of the
bleaching events would be expected to increase over time.
(b) If coral reefs were being stressed by other factors (e.g., nutrification, sedimentation,
physical damage), their tolerance of high temperatures might be reduced, again resulting in an
increasing frequency and severity of the bleaching events over time.
Source: Adapted from Williams and Bunkley-Williams, 1990a.
67
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Barnes, RD. 1968. Invertebrate zoology. Philadelphia, PA: W.B. Saunders Co.
Brown, BE, and Suharasono. 1990. Coral Reefs 8:163-170.
Bunkley-Williams, L, Morelock, J, and Williams, EH Jr. 1991. Lingering effects of the
1987 mass bleaching of Puerto Rican coral reefs in mid to late 1988. J. Aquatic Animal
Health 3:242-247.
Bunkley-Williams, L, and Williams, EH Jr. 1990. Global assault on coral reefs: What's
killing the great reefs of the world? Nat. Hist. (April 1990):47-54.
Carpenter, RC. 1990. Mass mortality of Diadema antillarum I: Long term effects on
sea urchin population-dynamics and coral reef algal communities. Mar. Biol. (Berl.)
104:67-78.
Causey, BD. 1988. Observations of environmental conditions preceding the coral
bleaching event of 1987. Proc. Assoc. Is. Mar. Labs. Carib. 21:48.
Cea-Egana, A, and DiSalvo, LH. 1982. Mass expulsion of zooxanthellae by Easter
Island corals. Pac. Sci. 36:61-63.
Cook, CB, Logan, A, and Ward, J, et al. 1990. Elevated temperatures and bleaching on
a high latitude coral reef the 1988 Bermuda event, North Atlantic Ocean. Coral Reefs
9:45-49.
Davis, GE. 1977. Anchor damage to a coral reef on the coast of Florida. Biol. Conserv.
11:29-34.
D'Elia, CF, Buddemeier, RW, and Smith, SV (eds.). 1991. Workshop on coral [reef]
bleaching reef ecosystems and global change: Report of proceedings. NSF/EPA/NOAA
Workshop 17-21 June, 1991. Maryland Sea Grant Report. 52 pp.
Dustan, P, and Halas, JC. 1987. Changes in the reef-coral community of Carysfoot
Reef, Key Largo, Florida: 1974 to 1982. Coral Reefs 6:91-106.
Gates, RD. 1990. Seawater temperature and sublethal coral bleaching in Jamaica West
Indies. Coral Reefs 8:193-198.
Glynn, PW. 1984. Widespread coral mortality and the 1982-1983 El Nino warming
event. Environ. Conserv. 11:133-146.
Glynn, PW. 1988. El Nino warming coral mortality and reef framework destruction by
echinoid bioerosion in the eastern Pacific. Galaxea 7:129-160.
68
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Glynn, PW. 1991. Coral reef bleaching in the 1980s and possible connections with
global wanning. Trends Ecol. Evol. 6:175-179.
Glynn, PW, and D'Croz, L. 1990. Experimental evidence for high temperature stress as
the cause of El Nino - coincident coral mortality. Coral Reefs 8:181-191.
Glynn, PW, and de Weerdt, WH. 1991. Elimination of two reef-building hydrocorals
following the 1982-83 El Nino warming event. Science 253:69-71.
Gomez, ED. 1988. Status of problems associated with coral reefs in the Pacific basin.
Coral Reef Newsletter 19:1-10.
Goreau, TJ, Hayes, RL, and Clark, JW, et al. 1992 (in press). Elevated sea surface
temperatures correlate with Caribbean coral reef bleaching. In: Geyer, RA (ed.). A
global warming forum: scientific, economic, and legal overview. Boca Raton, FL: CRC
Press.
Goreau, TJ, and MacFarlane, AH. 1990. Reduced growth rate oiMontastrea annularis
following the 1987 to 1988 coral-bleaching event. Coral Reefs 8:211-216.
Guzman, HM. 1991. Restoration of coral reefs in Pacific Costa Rica. Conserv. Biol.
5:189-.
Hayes, RL, and Bush, PG. 1990. Microscopic observations of recovery in the
reef-building scleractinian coral Montastrea annularis after bleaching on a Cayman reef.
Coral Reefs 8:203-210.
Holthus, PF, Maragos, JE, and Evans, CW. 1989. Coral reef recovery subsequent to the
freshwater kill of 1965 in Kaneohe Bay, Oahu, Hawaii, USA. Pacific Sci. 43:122-134.
Jackson, JB, Cubit, JK, and Keller, BD, et al. 1989. Ecological effects of a major oil
spill on Panamanian coastal marine communities. Science 243:37-44.
Jokiel, PL, and Coles, SL. 1990. Response of Hawaiian and other Indo-Pacific reef
corals to elevated temperature. Coral Reefs 8:155-162.
Lesser, MP, Stochaj, WR, and Tapley, DW, et al. 1990. Bleaching in coral reef
anthozoans effects of irradiance, UV radiation, and temperature on the activities of
protective enzymes against active oxygen. Coral Reefs 8:225-232.
Oliver, J. 1985. Recurrent seasonal bleaching and mortality of coral on the Great
Barrier Reef. Proc. 5th Intern. Coral Reef Sympos., Tahiti, 201-206.
69
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Pastorok, RA, and Bilyard, GR. 1985. Effects of sewage pollution on coral-reef
communities. Mar. Ecol. Prog. Ser. 21:175-189.
Porter, JW, Fitt, WK, and Spero, HJ, et al. 1989. Bleaching in reef corals physiological
and stable isotopic responses. Proc. Natl. Acad. Sci. USA 86:9342-9346.
Roberts, L. 1987. Coral bleaching threatens Atlantic reefs. Science 238:1228.
Roberts, L. 1988. Corals remain baffling. Science 239:256.
Rogers, CS. 1985. Degradation of Caribbean and Western Atlantic coral reefs and
decline of associated fisheries. Proc. 5th Intern. Coral Reef Sympos., Tahiti, 491-496.
Suharsono. 1988. Monitoring coral reefs to assess the effects of seawater warming in
1982-1983 at Pari Island Complex, Thousand Island, Indonesia. Abstr. 6th Intern. Coral
Reef Sympos., Australia, 97.
Szmant, AM, and Gassman, NJ. 1990. The effects of prolonged bleaching on the tissue
biomass and reproduction of the reef coral Montastrea annularis. Coral Reefs 8:217-224.
Walbran, PD, Henderson, RA, and Ml, AJ, et al. 1989. Evidence from sediments of
long-term Acanthaster planci predation on corals of the Great Barrier Reef. Science
245:847-850.
Webber, HH, and Thurman, HV. 1991. Bleaching of coral reef communities. In:
Marine biology. Harper Collins Publ. Pp 344-345.
Williams, EH Jr. 1991. Threat to black sea urchins. Nature 352:385.
Williams, EH Jr., and Bunkley-Williams, L. 1990a. The world-wide coral reef bleaching
cycle and related sources of coral mortality. Atoll Res. Bull. No. 335. Pp 1-72.
Williams, EH Jr., and Bunkley-Williams, L. 1990b. Coral reef bleaching alert. Nature
346:225.
Williams, EH Jr., and Grizzle, J. 1991. Coral reef bleaching. Marine ecological
disturbance information center. Lajas, PR: Department of Marine Sciences, University
of Puerto Rico. Summary 8, 15 June 1991.
Woodley, JD, et al. 1981. Hurricane Allen's impact on Jamaican coral reefs. Science
213: 749-755.
Yamaguchi, M. 1975. Sea-level fluctuations and mass mortalities of reef animals in
Guam, Mariana Islands. Micronesica 11:227-243.
70
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Yamazato, K. 1981. A note on the expulsion of zooxanthellae during summer 1980 by
the Okinawan reef-building corals. Sesoko Mar. Lab. Tech. Kept. 8:9-18.
2.4.5. Popular Press Bibliography
Booth, W. 1989. Oil slicks common three years after spill; even corals were killed in
mishap. Washington Post. November 19, 1989, vol 112, col 1, p A6.
Booth, W. 1991. Mysterious malady hits sea urchins. Washington Post. August 11,
1991, p A4.
Brower, K. 1989. State of the reef. Audubon 89:57-79.
Bunkley-Williams, L, and Williams, EH Jr. 1988. Coral reef Bleaching: Current crisis,
future warning. Sea Frontiers 34:80-87.
Carpenter, B. 1991. The ghosts of coral past. US News and World Report. September
23, 1991, pp 59-60.
Cowell, A. 1990. What next for fragile reef, a bridge? New York Times. March 9,
1990, vol 139, col 4, p A4.
Ford, J. 1988. Environmentalists criticize coral reef report. Japan Economic Newswire.
June 16, 1988.
Hollings, EF (Chairman). 1987. Bleaching of coral reefs in the Caribbean. Oral and
written testimony to the Commerce, Justice, State, Judiciary, and related agencies,
Appropriations Subcommittee, USA Senate (November 10).
Holman, RL. 1991. Pacific coral reefs damaged. Wall Street Journal. May 21, 1991, p
A18.
JEN. 1988. New airport plan threatens rare coral reef. Japan Economic Newswire.
February 5, 1988.
JEN. 1988. Rare coral reef will die in five years, experts say. Japan Economic
Newswire. May 13, 1988.
<^
Keating, D. 199f. Florida's barrier reef seen doomed by 2000; Some scientists dispute
finding of study. Washington Post.
Lauter, D. 1991. Florida Keys threatened by tourism; visitors and growth imperil water
quality, mangrove swamps, and coral reefs. Los Angeles Times. May 16, 1991, p 5.
71
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young terrestrial salamanders eat mites and insects that consume detritus;
and
adult salamanders prey on numerous organisms (e.g., worms, slugs, larval
and adult insects, and other salamanders).
Trends, Recently, the National Research Council (NRC) sponsored a workshop to
examine whether the numerous reported local extinctions and declines of amphibian
populations represent a worldwide phenomenon (NRC, 1990). The declines for some
populations, particularly of frogs, are as high as 50 to 90 percent and are occurring even
in relatively pristine habitats
such as national parks and
biological preserves (Blaustein
and Wake, 1990). Examples of
declining amphibian
populations in North America
and elsewhere are provided in
Exhibits 2.5.1 and 2.5.2,
respectively.
Although formal analyses
are not yet available, the
number of investigators
reporting similar trends leads
credence to the hypothesis that
amphibians in general are
suffering population declines
worldwide. Many of the
declines can be attributed to
obvious habitat destruction or
modification. However, the decline of populations in protected areas indicates that
other, more global, factors also may be involved.
Not all species are declining, however. For example, there is no indication that
frog populations in the vicinity of the Savannah River Laboratory have declined over the
past 11 years (Pechmann and Scott, 1990), nor have frog populations in monitored
Borneo streams declined (Robert Inger as reported by Blaustein and Wake, 1990).
Declines are being noted primarily in temperate or higher latitudes and in higher
elevations. There is little evidence for declines of amphibians within 10° latitude north or
south of the equator or low-altitude regions, aside from the dramatic losses resulting
from complete habitat destruction associated with deforestation, urban development, and
destructive agricultural practices (Blaustein and Wake, 1990).
- _
74
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Exhibit 2.5.1. Examples of declining amphibian populations in North America.
The western spotted frog is now absent from over one third of its 1970's range in
Oregon (Andrew Blaustein as reported by Blaustein and Wake, 1990).
The red-legged frog, once abundant in western states (Jennings, 1988), is now
extinct in Oregon (Blaustein and Wake, 1990) and southern California (Marc
Hayes as reported in Blaustein and Wake, 1990) and is declining elsewhere in
California (Jennings, 1988).
The Cascade frog is declining in Oregon (Blaustein and Wake, 1990).
The mountain and foothill yellow-legged frog and the Yosemite toad are declining
not only in the mountain and foothills of California, but also in the lakes in Kings
Canyon and Sequoia National Parks in California (David Bradford as reported by
Blaustein and Wake, 1990; Jennings, 1988; Jennings as reported by Cowen, 1990).
The boreal toad (Bury and Corn as reported by Cowen, 1990), Wyoming toad
(Baxter and Meyer, 1982), chorus frog, leopard frog (Corn and Fogleman, 1984),
woodfrog, and tiger salamander have declined markedly in the Rocky Mountains of
Colorado (Vaughan Shoemaker as reported by Blaustein and Wake, 1990; Corn
and Fogleman, 1984; Harte and Hoffman, 1989). For example:
The leopard frog (Rana pipiens) inhabits only 4 of 33 sites where it was
once abundant, and
The boreal toad is seen in just 10 of 59 areas that it had frequented
previously (Bury and Corn as reported by Cowen, 1990).
On the Huyck Preserve and Biological Research Station in the Helderberg Plateau
in New York, four species of amphibians that were recorded on the Preserve in
1938 no longer occur there (Wyman, 1988b).
Although population-level effects are not yet documented, the western toad
recently has suffered severely reduced reproductive success in Lost Lake of the
Oregon Cascade Mountains. Egg mortality rates in 1989, 1990, and 1991 were
50%, 100%, and 50%, respectively, whereas egg mortality rates never had
exceeded 5% in the previous 11 years the lake was monitored (Blaustein and
Olson, 1991).
75
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Exhibit 2.5.2. Examples of declining amphibian populations in other areas.
• At the University of Sao Paolo's field station at Boracea, Brazil, 6 of 30 frog
species have disappeared since 1982 and 7 have declining populations CHeyer et
al., 1988).
• The gastric brooding frog, discovered in large numbers (i.e., many hundreds) in
1974 by Michael Tyler of the University of Adelaide, Australia, completely
disappeared from its range (the Conondale Ridges area) by 1981 (Blaustein and
Wake, 1990).
• The range of the natterjack toad (Bufo calamitd) in Britain has shrunk by fifty
percent in recent years (Beebee et al., 1990).
• The golden toad in Monteverde Cloud Forest Preserve, Costa Rica, has declined
from around 1,000 breeding individuals in the early 1980's to a few by the mid to
late 1980's (about a dozen according to Marc Hayes as reported by Blaustein and
Wake, 1990; one frog only according to Martha Crump as reported by Barinaga,
1990).
• Salamanders near Oaxaca, Mexico, appear to be declining (Barinaga, 1990).
• In the Venezuelan Andes, "drastically diminished" populations of five species of
Atelopus toads recently have been reported (La Marca and Reinthaler, 1991).
76
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2.5.2. Hypotheses
Several explanations of a possible worldwide decline in amphibian populations are
being considered in the scientific community:
• destruction of natural habitats;
• acid deposition (i.e., deposition of nitrates, sulfates, ammonia, and hydrogen);
• introduced species (i.e., competition and predation by bullfrogs, and predation by
introduced fish species);
• unusual climatic variations (i.e., unusually cold winters and dry summers);
• exploitation by humans (e.g., food, research, pet trade);
• widespread use of pesticides and toxic substances;
• pathogens;
• increased ultraviolet radiation;
• synergistic interactions among the above factors; and
• natural cyclic fluctuations in populations.
In general, distinguishing human-induced trends from natural variation in
amphibian populations is difficult (Pough as reported by Blaustein and Wake, 1990;
Pechman et al., 1991; Wake, 1991). Moreover, there are few quantitative baseline data
by which to judge recent changes (Barinaga, 1990; Blaustein and Wake, 1990; Vitt et al.,
1990). To date, much of the evidence of declining population comes from the anecdotal
personal experiences of herpetologists and other biologists, rather than experimental
design (Young, 1990). We discuss the hypotheses listed above in the following
paragraphs.
Destruction of natural habitats. An indisputable contribution to the decline of
many amphibian species is habitat destruction. Beyond outright destruction of habitats,
remaining surface waters and wetlands can be so modified as to be no longer suitable
habitat for native species. Changes that increase temperature, eliminate suitable
oviposition (i.e., egg-laying) sites, refuges, and hibernating areas are particularly
important to amphibians. On a global scale, a large proportion of the habitat used by
amphibian species is being lost due to tropical deforestation (Wyman, 1991; Blaustein
and Wake, 1990). Habitat alteration also has been suggested as a major factor
77
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contributing to the decline of frog species in western North America (Moyle, 1973; Bantu
and Morafka, 1966, as cited in Hayes and Jennings, 1986). For example:
Dam and reservoir building and mining result in removal of riparian (i.e., along
the edge of rivers and streams) vegetation and decreases in stream flow, which in
turn result in increased water temperature beyond the optima or tolerance range
of many species (Bury and Corn, 1988a,b; Corn and Bury, 1989; Hayes and
Jennings, 1986; Jennings, 1988);
Livestock grazing can produce similar results, i.e., removing vegetative cover,
increasing ambient water temperatures, and eliminating desirable undercut banks
(Jennings, 1988);
Logged forests increase sedimentation in streams, reducing habitat for larval
salamanders and frogs (Bury and Corn, 1988a; Corn and Bury, 1989). [Corn and
Bury (1989) found species richness to be highest in streams in uncut forests and
density and biomass of individual species to be significantly reduced in streams in
logged forests (Exhibit 2.5.3.];
Logging, clear-cutting, and roads cause obvious fragmentation of habitat suitable
for amphibians. Patches of high soil acidity also may preclude movements of
amphibians from one stream or, pond to the next (Wyman, 1991); and
Habitat fragmentation also may increase the probability of local population
extinctions as a result of natural or other extremes in temperature or precipitation
(Wyman, 1991; Jennings, 1988).
Nonetheless, the most disconcerting
aspect of the apparent global decline in
amphibian species is that declines have
been observed in populations that are not
subject to overt habitat destruction. The
following sections review hypotheses to
explain this phenomenon. Given the
recent recognition of the problem, none
of the following hypotheses has been
extensively developed or investigated.
Acid deposition. Acid deposition,
including dry deposition and deposition
from snow melt, can have various adverse
effects on amphibians. Many
salamanders, toads, and frogs breed in
temporary pools formed in the early
78
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Exhibit 2.5.3. Effect of logging on amphibian species number and density in western
Oregon.
(a)
50 -,
tn
UNCUT FOREST
LOGGED FORESTS
01234
NUMBER OF AMPHIBIAN SPECIES IN STREAM
-------
spring by melting snow and rain (Freda, 1986; Freda et al., 1991; Pough, 1976). These
breeding ponds are generally small, low in acid buffering capacity, and darkly stained by
humic substances. These factors increase the potential for acidification and make it
difficult to distinguish the contribution of acid from anthropogenic factors (e.g.,
atmospheric deposition) from that of natural sources (e.g., sphagnum and organic acids)
(Freda, 1986; Pough, 1976). Acidified soils also can stress terrestrial forms (e.g., toads,
salamanders) and life stages (e.g., efts), particularly in areas with low soil buffering
capacity (Wyman, 1991). Acidic soils apparently contribute to the loss of sodium and
water from amphibians, resulting in a sodium and water deficit (Frisbie and Wyman,
1991). When conditions dry during droughts, soils become more acidic and amphibians
lose water both as a consequence of the dry conditions and the loss of sodium, which is
followed by more water loss (by osmosis) (Frisbie and Wyman, 1991). The synergistic
effects of low soil moisture, low pH, and high temperatures may produce lethal water
stress on terrestrial amphibians (Wyman, 1991).
Investigators have documented several ways in which acid deposition can have
adverse effects on amphibians. Acid influx during spring snow melts can acidify breeding
ponds to levels that cause death in embryos (Harte and Hoffman, 1989; Pough, 1976;
Pough and Wilson, 1977) and larvae (Saber and Dunson, 1978). Harte and Hoffman
(1989) suggested that acid spring snow melts were responsible for the 65 percent decline
of a Rocky Mountain population of the tiger salamander (Ambystoma tigrinuni); however,
this finding recently has been disputed (Scott Wissinger, unpubl. data, Wyman, pers.
comm.). Chronic acid surface water conditions can inhibit sperm mobility and cause
developmental abnormalities in embryos (Gosner and Black, 1957; Pough and Wilson,
1977; Cook, 1983; Pierce, 1985; Schlichter, 1981). Acidic conditions also can slow or
inhibit development of eggs (Harte and Hoffman, 1989; Pough, 1976), and tadpoles
(Beebee et al., 1990; Freda and Dunson, 1986; Pierce and Montgomery, 1989) (Exhibit
2.5.4). Slower developmental rates increase the chances of predation and failure to
metamorphose from tadpole to frog before the pond dries out. Freda and Dunson
(1985) found that sodium loss is increased and total body sodium reduced in amphibian
larvae exposed to acidic water. The larvae die when about half of the body's sodium
content has been lost. The same problem may affect terrestrial salamanders (Frisbie and
Wyman, 1991; Wyman, 1991). Interactions between pH and other chemical and physical
variables (e.g., temperature, concentrations of aluminum, calcium, and organic acids) may
cause variability in amphibian mortality at specified pH levels (Freda, 1986; Freda and
Dunson, 1986).
Amphibian species show a range of sensitivities to acidic conditions. Those
species that breed in naturally more acidic conditions appear to be more resistant to acid
(Pierce, 1985). Acid-sensitive species tend to be absent from acidic ponds (Freda and
Dunson, 1986) and salamanders have been shown to avoid areas of low pH soils (Wyman
and Hawksley-Lescault, 1987). Adults of at least 10 species of amphibians show
distributions and densities that are positively correlated with soil pH (Wyman, 1988a;
80
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Exhibit 2.5.4. Acid tolerance of natterjack toad development.
100 -,
75 -
o 50 -
25 -
0%
<4.0
89%
25%
96%
100%
4.0-5.0 >5.0-6.0
pH Range
95%
>6.0
Hatch Rate
Survival to Metamorphosis
Low pH reduces hatch rate and survival to metamorphosis in natterjack toads. Growth rate
also is reduced at low pH.
Source: Adapted from Beebee et al., 1990.
81
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Wyman and Hawksley-Lescault, 1987; Wyman, 1991). Wyman (1988a) also found a
strong negative correlation between the number and density of species of amphibians in a
forested habitat and the acidity of the soil. Available evidence links the loss of the
natterjack toad from lowland heaths that formerly supported about half of the British
population to recent acidification of this habitat (Beebee et al., 1990).
In summary, acidified surface waters have been shown to have adverse effects on
developing embryos and larvae, and acid deposition has been implicated in the decline or
reduced range of some terrestrial as well as aquatic species and life stages. The extent to
which acid deposition and concurrent changes in water and soil chemistry may be
responsible for other species declines is not known.
Introduced species. Several investigators have suggested that bullfrogs and
introduced carnivorous fish may be contributing to declines of amphibian populations in
the United States, particularly in the western states. Bullfrogs were first introduced to
western North America in California in 1896 (Heard, 1904*P, as cited in Hayes and
Jennings, 1986). Over 60 species of fishes, have been introduced to western North
America over the past 120 years, and of these, 59 percent are predatory (Hayes and
Jennings, 1986; Jennings, 1988). We discuss the evidence for concerning bullfrogs and
fish separately below.
Bullfrogs. Changing land-use patterns in the United States have resulted in
favorable habitat for bullfrogs and increased competition of native frog
populations with bullfrogs (Corn and Fogleman, 1984; Hammerson, 1982; Hayes
and Jennings, 1986). Some investigators (e.g., Dumas, 1966; Hammerson, 1982;
Moyle, 1973) claim that several frog species' populations are declining in the west
at least in part because of bullfrogs. The most frequently cited of these, Moyle
(1973), reported that the two frog species that used to be the most common in the
San Joaquin Valley of California are now absent or rare, while the bullfrog has
become the dominant frog on the valley floor and has spread to the surrounding
foothills. The native species are found only in areas where the bullfrog is absent.
The evidence implicating bullfrogs as the cause of declining populations of frogs in
the western United States cited by Moyle (1973) includes:
• The sizes of frog and bullfrog populations tend to be inversely correlated;
• Bullfrogs are the most frequently encountered Ranid (i.e., true frog) species
in many areas;
• Bullfrogs occupy areas once inhabited by declining species of frogs; and
• Bullfrogs are known to eat juvenile frogs of other species when both are in
captivity.
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The bullfrog hypothesis is not universally accepted, however, because predation
has not been observed in the field (Hayes and Jennings, 1986), and because the
appropriate competition and predation experiments have not yet been conducted
to test the hypothesis critically (Jennings, 1988).
Fish. In California and other western states, frogs originally evolved with little
pressure from fish predation and may not have any natural defense mechanisms
against fish predators. About 8 of 50 introduced fish species that have become
most extensively naturalized in the west are carnivorous, and some are known to
prey on frogs (Hayes and Jennings, 1986). Two types of evidence support the role
of introduced fish species in the decline of western frogs: (1) an inverse
relationship between the abundance of introduced fishes and the abundance of
endemic frogs (i.e., frog species found only in that area); and (2) the fact that
many of the introduced fish are specialized to feed on aquatic life (e.g., amphibian
eggs and larvae) (Jennings, 1988). Hayes and Jennings (1986) believe that in the
absence of adequate data, available information suggests that the introduction of
alien fish species may be more important than the introduction of bullfrogs in
contributing to the decline of frog species in western North America.
Unusual climatic variations. Unusually cold winters or dry summers may have
contributed to local declines and extinctions of amphibian populations. For example,
unusually heavy frosts in recent years may account for the widespread extent of declines
in southeast Brazil (Heyer et al., 1988). The severe drought of the mid-1970's caused
large areas of amphibian breeding habitat to dry up, resulting in reproductive failure of
the northern leopard frog in Colorado (Corn and Fogleman, 1984; Hayes and Jennings,
1986). Whether these events represent natural extremes in weather patterns or have
resulted from the effects of human activities on regional and global climate is unknown.
Wyman (1991) recently suggested that global climate change may be contributing
to the general amphibian decline. He surveyed 25 herpetologists active in the
northeastern United States for their opinions on the causes of declining species in this
region. Although the survey results represent largely subjective impressions, the
herpetologists cited "problems at the edge of the range" as a major cause for the declines
of 12 of the 19 species identified as declining over part or all of their ranges. Wyman
pointed out that the first areas in which one would expect to see population declines as a
result of global climate changes would be at the edge of species' ranges. These also are
the areas where natural, cyclic fluctuations would be most pronounced.
Exploitation by humans. Frogs have periodically been exploited for food by several
cultures in many areas. Alain Dubois of the Natural Museum of History in Paris points
out that the French consumption of frogs legs has been linked to a marked decline of
native frogs in Europe, India, and Bangladesh (as cited by Blaustein and Wake, 1990).
The red-legged frog was heavily exploited in the western United States in the late 1800's,
which contributed to its initial decline, although exploitation does not explain the
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continued loss (Jennings, 1988). This hypothesis does not apply to most of the declining
populations of amphibians, however.
Widespread use of pesticides and other toxic substances. Species with "amphibious"
life histories, i.e., whose life cycle require both terrestrial and aquatic habitats, can be
particularly vulnerable to environmental pollutants (NRC, 1990; Norse, 1990). The eggs
of many amphibians are laid in water and have little physical protection from water-
borne contaminants. Many species' larval stages are also aquatic. Adult amphibians are
carnivorous and therefore vulnerable to toxic substances that tend to biomagnify in food
chains (e.g., mercury, PCBs).11 In addition, amphibians' skin is permeable to airborne
gases as well as many soil- and water-borne contaminants.
Amphibians are sensitive to the usual variety of toxic substances (Power et al.,
1989). To date, however, the evidence that pesticides and toxic substances are
contributing to a large-scale decline in amphibian populations is limited. Baxter and
Meyer (1982) have stated that aerial application of pesticides caused some of the
declines of leopard frog in Wyoming (Corn and Fogleman, 1984). Although it is known
that larval stages of some species are particularly sensitive to toxic substances (Hayes and
Jennings, 1986), definitive studies linking environmental contamination with reduced
populations of larval stages are lacking at this time.
Pathogens. Although epizootics (e.g., diseases) are of concern in declining
populations of several groups of organisms, (e.g., cholera and botulism in waterfowl,
distemper in seals), wild frog population responses to pathogens and parasites are
essentially unstudied (Hayes and Jennings, 1986). Lucke tumor herpesvirus (LTHV),
which causes renal carcinomas (malignant) in frogs, was prevalent a decade ago when
leopard frog population densities were high. Leopard frog populations subsequently
declined, but tumor incidence is increasing again after an absence for 10 years despite
low population densities (Hunter et al., 1989). Recent data from Pennsylvania suggests a
synergistic effect of low pH stress and bacterial infections in declining frog species in this
state (Simon, as described by Wyman, pers. comm.). Possible contributions of other
pathogens to amphibian population declines have not been studied, nor has the potential
for interaction of pathogens and other stresses been evaluated.
Increased ultraviolet radiation. The exposed skin of amphibians could render them
more sensitive to increased ultraviolet radiation than other vertebrate groups. However,
higher UV levels have not been measured in association with declining amphibian
populations as yet (Barinaga, 1990).
Synergistic effects among factors. Synergistic effects may result from more than one
of these stresses. As soils dry, they become more acidic, increasing the water stress on
11See footnote number 5, page 49.
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amphibians (see Acid deposition above)
(Wyman, 1991). Amphibians also are
more sensitive to heat stress in the
absence of water. Drought, heat, and
acidity represent potentially significant
stressors when occurring together
(Wyman, 1991).
Natural, cyclic fluctuations. Animal
populations fluctuate in size due to
natural changes in food supply, predation,
competition, pathogens, and abiotic
conditions such as weather. Some
fluctuations after unusual events such as
prolonged drought or early frosts may
seem catastrophic. For example, census
data from 1979 to 1990 for three salamander species and one frog species at a breeding
pond in South Carolina showed extreme fluctuations in population size from year to year,
but no overall trend over the 11 years (except for one population which increased
slightly; Pechmann et al., 1991). Thus, at any given time, one would expect a number of
populations worldwide to be in decline, others to be stationary, and still others to be
increasing. Anthropogenic stresses may exacerbate naturally-initiated declines in
populations, but distinguishing which fluctuations may be outside the range of natural
variation is difficult because of the large number of factors and interactions involved.
2.5.3. Continued Monitoring
The International Union for the Conservation of Nature (IUCN) recently set up a
"Declining Amphibian Populations Task Force" at the Environmental Research
Laboratory in Corvallis, Oregon. The Task Force is trying to set up a worldwide
communication network and to establish a database for all scientists involved in
amphibian research (Vial, 1992). The Task Force also is to organize a global monitoring
program for (1) determining the status of amphibian populations, (2) assessing the
implications of any declines, (3) studying potential causative factors, and (4) making
appropriate policy recommendations based on these findings.
Several meetings focused on the declining amphibian population issue have been
held in the past year. In August, 1991, a symposium was held at the annual meeting of
the Society for the Study of Amphibians and Reptiles to discuss "Amphibian Declines
and Habitat Acidification." Resulting papers will be published in the Journal of
Herpetology. A workshop on "Declines in Canadian amphibian populations; designing a
national monitoring strategy" was held in Canada in October 1991. Regional Working
Groups of the Task Force also have been holding meetings.
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2.5.4. References
Banta, BH, and Morafka, DJ. 1966. An annotated checklist of the recent amphibians
and reptiles inhabiting the city and county of San Francisco, California. Wasmann J.
Biol. 24:223-238.
Barinaga, M. 1990. Where have all the froggies gone? Science 247:1033-1034.
Baxter, GT, and Meyer, IS. 1982. The status and decline of the Wyoming toad. J.
CO-WY Acad. Sci. 14:33.
Beebee, TJ, Flower, RJ, and Stevenson, AC, et al. 1990. Decline of the natterjack toad
Bufo-Calamita in Britain, UK: Paleoecological documentary and experimental evidence
for breeding site acidification. Biol. Conserv. 53:1-20.
Blaustein, AR, and Olson, DH. 1991. Declining amphibians (letter). Science 253:1467.
Blaustein, AR, and Wake, DB. 1990. Declining amphibian populations, a global
phenomenon. Trends Ecol. Evol. 5:203-204.
Burton, TM, and Likens, GE. 1975. Salamander populations and biomass in the
Hubbard Brook Experimental Forest, New Hampshire. Copeia 1975:541-546.
Bury, RB, and Corn, PS. 1988a. Aquatic and streamside amphibians. In: Streamside
management: Riparian wildlife and forestry interactions, Seattle, WA: University of
Washington, Institute of Forest Resources, Contribution No. 59.
Bury, RB, and Corn, PS. 1988b. Douglas-fir forests in the Oregon and Washington
Cascades: Relation of the herpetofauna to stand age and moisture. In: Proceedings:
Management of Amphibians, Reptiles, and Small Mammals in North America, Flagstaff,
AZ, July 19-21, 1988. Pp. 11-21.
Cook, RP. 1983. Effects of acid precipitation on embryonic mortality ofAmbystoma
salamanders in the Connecticut Valley of Massachusetts. Biol. Conserv. 27:77-88.
Corn, PS, and Bury, RB. 1989. Logging in western Oregon: Responses of headwater
habitats and stream amphibians. Forest Ecol. Manage. 29:39-57.
Corn, PS, and Fogleman, JC. 1984. Extinction of montane populations of the northern
leopard frog (Rana pipiens) in Colorado. J. Herp. 18:147-152.
Cowen, R. 1990. Tales from the Froglog and others. (Amphibian population declines).
Science News 137:158.
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Dumas, PC. 1966. Studies of the Rana species complex in the Pacific Northwest.
Copeia 1966:60-74.
Freda, J. 1986. The influence of acidic pond water on amphibians: A review. Water Air
Soil Poll. 30:439-450.
Freda, J, and Dunson, WA. 1985. Field and laboratory studies of ion balance and
growth rates of Ranid tadpoles chronically exposed to low pH. Copeia 1985:415-423.
Freda, J, and Dunson, WA. 1986. Effects of low pH and other chemical variables on
the local distribution of amphibians. Copeia 1986:454-466.
Freda, J, Sadinski, W, and Dunson, WA. 1991. Long term monitoring of amphibian
populations with respect to the effects of acidic deposition. Water Air Soil Poll.
55:445-462.
Frisbie, and Wyman, R. 1991. Effects of soil pH on sodium balance in the red-backed
salamander, Plethodon cinereus, and three other salamanders. Physiol. Zool.
Gosner, KL, and Black, IH. 1957. The effects of acidity on the development and
hatching of New Jersey frogs. Ecology 38:256-262.
Hammerson, GA. 1982. Bullfrog eliminating leopard frogs in Colorado? Herpetol. Rev.
13:115-116.
Harte, J, and Hoffman, E. 1989. Possible effects of acidic deposition on a Rocky
Mountain population of the tiger salamander Ambystoma tigrinum. Conserv. Biol.
3:149-158.
Hayes, MP, and Jennings, MR. 1986. Decline of ranid frog species in western North
America: Are bullfrogs (Rana catesbeiana) responsible? J. Herpetol. 20:490-509.
Heyer, WR, Rand, AS, and Goncalvez, CA, et al. 1988. Decimation extinctions and
colonizations of frog populations in southeast Brazil and their evolutionary implications.
Biotropica 20:230-235.
Hunter, BR, Carlson, DL, and Seppanen, ED, et al. 1989. Are renal carcinomas
increasing in Rana pipiens after a decade of reduced prevalence? Am. Midi. Nat.
122:307-312.
Jennings, MR. 1988. Natural history and decline of native ranids in California. In: Le
Lisle, HJ, Brown, PR, and Kaufman, B, et al., (eds.), Proceedings of the Conference on
California Herpetology, Southwestern Herpetologists Society. Pp. 61-72.
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La Marca, E, and Reinthaler, HP. 1991. Herp. Rev. 22:125-128.
Moyle, PB. 1973. Effects of introduced bullfrogs, Rana catesbeiana, on the native frogs
of the San Joaquin Valley, California. Copeia 1973:18-22.
Norse, E. 1990. EPA and Biological Diversity Part 1: Threats to Biological Diversity in
the United States. Washington, DC: Environmental Protection Agency, Science Policy
Integration Branch, Office of Policy Analysis.
NRC. 1990. Findings and recommendations. From: Workshop on: Declining
amphibian populations - A global phenomenon?, Arnold and Mabel Beckman Center,
Irvine, CA, February 19-20, 1990. National Research Council. Pp. 1-10.
Pechmann, JH, Scott, DE, and Semlitch, RD, et al. 1991. Declining amphibian
populations: The problem of separating human impacts from natural fluctuations.
Science 253:892-895.
Pechmann, JH, and Scott, DE. 1990. Are amphibian populations declining? Data from
a temporary pond in South Carolina, USA. Bull. Ecol. Soc. Am. 71:282.
Pierce, BA, and Montgomery, J. 1989. Effects of short-term acidification on growth
rates of tadpoles. J. Herpetol. 23:97-102.
Pierce, TK. 1985. Acid tolerance in amphibians. BioSci. 35:239-243.
Pough, FH. 1976. Acid precipitation and embryonic mortality of spotted salamanders,
Ambystoma maculatum. Science 192:68-70.
Pough, FH, and Wilson, RE. 1977. Acid precipitation and reproductive success of
Ambystoma salamanders. Water Air Soil Poll. 7:531-544.
Power, T, Clark, KL, and Harfenist, A, et al. 1989. A review and evaluation of the
amphibian toxicological literature. Canadian Wildlife Service Technical Report No. 61.
Saber, PA, and Dunson, WA. 1978. Toxicity of bog water to embryonic and larval
anuran amphibians. J. Exp. Zool. 204:33-42.
Schlichter, L. 1981. Low pH effects the fertilization and development of Rana pipiens
eggs. Can. J. Zool. 59:1693-1699.
Vial, JL (ed). 1992. Froglog; IUCN/SSC Declining Amphibian Populations Task Force.
Number 1, March, 1992.
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Vitt, LJ, Caldwell, JP, and Wilbur, HM, et al. 1990. Amphibians as harbingers of decay.
BioSci. 40:418.
Wake, DB. 1991. Declining amphibian populations. Science 253:860.
Wyman, RL. 1988a. Soil acidity and moisture and the distribution of amphibians in five
forests of southcentral New York. Copeia 1988:394-399.
Wyman, RL. 1988b. Occasional Paper #1, A history of research and a description of
the biota and ecological communities of the Edmund Niles Huyck Preserve and
Biological Research Station. Rensselaerville, NY: EN Huyck Preserve.
Wyman, R. 1990. What's happening to the amphibians? Conserv. Biol. 4:350-352.
Wyman, RL. 1991. Multiple threats to wildlife: Climate change, acid precipitation, and
habitat fragmentation. In: Global climate change and life on earth, New York, NY:
Chapman and Hall.
Wyman, RL, and Hawksley-Lescault, D. 1987. Soil acidity affects distribution, behavior,
and physiology of the salamander Plethodon cinereus. Ecology 68:1819-1827.
Young, S. 1990. Twilight of the frogs. New Scientist (April):27.
2.5.5. Popular Press Bibliography
Anonymous. August 1991. New task force on declining amphibians. Science 509.
Beardsley, T. 1991. Murder mystery. Sci. Amer. (Nov):29.
Booth, W. 1990. Frogs, toads vanishing across much of the world; 'Environmental
degradation' may be to blame, scientists say. Washington Post. February 9, 1990. p Al.
Borchelt, R. 1990. Frogs, toads, and other amphibians in distress. News Rept.
(April):2-5.
Cowell, A. 1990. Spring peepers sound and eco-warning. Christian Science Monitor.
January 8, 1990, vol 82, No 118, col 1, p 12.
Detjen, J. 1990. Disturbing decline among amphibians puzzles researchers. Philadelphia
Inquirer. September 25, 1990, pp 1A, 8A.
Ford, P. 1991. Hard times for frogs. Country Journal 18:46-49.
Heard, M. 1904. A California frog ranch. Out West 21:20-27.
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Hillinger, C. 1991. Toad tracking. (Los Padres National Forest arroyo toads threatened
with extinction). Los Angeles Times. May 3, 1991, p A3.
Hillinger, CH. 1991. Recent rain saves rare amphibians, but scientist sees threat of
extinction. Los Angeles Times. May 3, 1991, p A3.
Lawren, B. 1991. Mystery of the frogs. Good Housekeeping 212:91.
Milstein, M. 1990. Unlikely harbingers. National Parks 64:18-24.
Phillips, K. 1990. Where have all the frogs and toads gone? BioSci. 40:422-424.
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2.6. Turtles Worldwide
Summary. Approximately one third of the world's species of land turtles
(terrestrial and freshwater semi-aquatic) are now considered to require conservation
attention. All of the world's sea turtle species are considered threatened or endangered.
For the land turtles, habitat destruction and fragmentation appear to be the primary
causes. Juvenile and adult sea turtles suffer primarily from capture by shrimp trawlers,
but other factors also cause excess mortality. Various human activities on nesting
beaches have reduced the survivorship of sea turtle eggs and hatchlings.
Background. The turtles represent one of the most ancient groups of animals,
having survived from before the age of the dinosaurs, or over 150 to 200 million years
(Behler and King, 1979). Of the land turtles, snapping turtles, musk and mud turtles,
and pond turtles are primarily aquatic, inhabiting a variety of freshwater habitats. Box
turtles and tortoises represent the primarily terrestrial land turtles. Sea turtles feed at
sea, but lay their eggs onshore. Because the principal causes of declining populations
differ for land and sea turtles, we discuss them separately in Sections 2.6.1 and 2.6.2,
respectively.
2.6.1. Land Turtles
2.6.1.1. Description
Background. Both
freshwater semi-aquatic and
terrestrial turtles and tortoises
lay their eggs in "nests" dug on
dry ground. Suitable nesting
sites (i.e., appropriate soil
texture and conditions) may be
some distance from the turtles'
normal foraging habitat, and
females may need to travel
some distance to lay their eggs.
Both aquatic and terrestrial
turtles are relatively slow
moving on land, making them
vulnerable to mortality on
roadways during dispersal
movements and during travel to
locate nest sites. Turtles also
tend to be long-lived with.a low yearly reproduction rate, characteristics that make
recovery from population declines difficult.
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Exploitation by humans. Turtles and tortoises are used for food by numerous
cultures in developing countries (Bury, 1982; Morafka, 1982; Stevens, 1990*P), and
several species are heavily utilized in the pet trade (Bury, 1982) or simply collected for
pets (Luckenbach, 1982). Data to quantify these losses are not readily available,
however.
2.6.2. Sea Turtles
2.6.2.1. Description
Background. Sea turtles breath air, and therefore tend to swim near the surface of
the ocean. They lay their eggs on dry land to incubate, generally on a small number of
suitable "laying beaches." Once the eggs hatch, the juvenile turtles must be able to reach
the sea using light cues for orientation.
Trends. All of the eight sea turtle taxa of the world now require conservation
attention and all of the five sea turtle species that breed in US coastal areas are
Federally designated as endangered or threatened (NAS, 1990). Exhibit 2.6.2 lists
population trends for several species of sea turtle for which adequate long-term data are
available. For example, on the Mexican coast of the Gulf of Mexico where 40,000
Kemp's ridley turtles were observed nesting on a single day in 1947, the total population
of nesting females now may be no more than 350 (NAS as reported by Abramson,
1990*P).
2.6.2.2. Hypotheses
Recently, the National Academy of Science's (NAS) Committee on Sea Turtle
Conservation reviewed factors that threaten the five sea turtle species found in coastal
United States' waters. These and other factors are likely to threaten sea turtles
worldwide. We describe factors that cause increased mortality of eggs and hatchlings on
land and factors that increase juvenile and adult mortality at sea separately in the next
two subsections.
Mortality of Eggs and Hatchlings
Numerous human activities can cause increased levels of mortality in sea turtle
eggs and hatchlings on land: beach erosion and accretion, beach armoring, artificial
lighting, beach nourishment and cleaning, increased human presence, recreational beach
equipment and vehicles, introduced non-native dune and beach vegetation, and direct
hunting. We discuss each of these hypotheses briefly below.
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Exhibit 2.6.2. Sea turtle population trends.
Species
Kemp's ridley
Loggerhead
Green turtle
Hawksbill
Leatherback
Location
Mexico
Georgia, US
South Carolina, US
Florida, US
Florida, US
Surinam
Costa Rica
Surinam
Puerto Rico
Virgin Islands
From To Population Change
1947 1988 -99%
1963 1989 -70%
1973 1989 -71%
1981 1989 NSC
1971 1989 +100%
1968 1981 NSC
1971 1987 NSC
insufficient time series
insufficient time series
insufficient time series
All values approximate; estimated from figures. NSC = no significant change.
Source: NAS, 1990.
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Beach erosion and accretion. Coastal development has increased erosion rates and
interrupted natural shoreline migration, which results in loss of suitable nesting habitat
(NAS, 1990). In Florida, where 90 percent of the loggerheads in the Western
Hemisphere nest, eroding beaches may present one of the greatest long-term threats to
the species (R.H. Spadoni, as reported by Dean, 1992*P).
Beach armoring. Shoreline development such as sea walls, rocks revetments,
riprap, sandbags, and jetties, causes loss of beach area, increased amounts of debris
onbeaches, and beach erosion. These factors in turn result in loss of sea turtle nesting
habitat, restricted female access to suitable nesting sites, and can cause turtles to
abandon nests or construct egg cavities of improper size and shape (NAS, 1990).
Artificial lighting. Sea turtle hatchlings use light as a cue to find the sea following
hatching (Daniel and Smith, 1947; Carr and Ogren, 1960 as cited by NAS, 1990).
Artificial light from buildings, streetlights, dune crossovers, or vehicles can disorient
hatchlings potentially resulting in death (McFarlane, 1963; Philibosian, 1976; Ehrhart,
1983; as cited in NAS, 1990; Witherington and Bjorndal, 1991). Also, adult females have
been found to avoid nesting areas because of light (NAS, 1990).
Beach nourishment and cleaning. The deposition of sand (beach nourishment) to
replace sand lost by erosion can result in severe compaction, inhibiting or preventing nest
digging (Raymond, 1984). The composition of the deposited sand may differ from native
sand, reducing hatching success (NAS, 1990). Both of these factors have been found to
inhibit successful reproduction of sea turtles (NAS, 1990). Cleaning of beaches can
disturb nests and hinder or trap emergent hatchlings.
Increased human presence. Human activities on the beach, particularly in the
evening and at night, can disturb female sea turtles as they try to dig their nests and lay
eggs (Hosier et al., 1981; NAS, 1990).
Recreational beach equipment and vehicles. Vehicles on the beach deter nesting
attempts, destroy clutches, and interfere with the seaward journey of hatchlings (NAS,
1990).
Non-native dune and beach vegetation. In the United States, the introduced
Australian pine has increased beach shading, which lowers sand temperatures and may
alter the normal sex ratio of the hatchlings, which is temperature-dependent (NAS, 1990).
Other species of introduced vegetation have disrupted sea turtle nesting success because
of increased root mats and erosion (NAS, 1990).
Direct taking of eggs. Direct taking of eggs is seldom reported in the United States.
In some other countries, however, eggs are taken in large numbers. For example, in
Mexico in 1989 alone, an estimated 10 million sea turtle eggs were gathered illegally by
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poachers on government protected beaches and sold for supposed aphrodisiac properties
(H. Aridjis, as reported by Branigin, 1990*P).
Mortality of Juveniles and Adults
The most important source of mortality for juvenile and adult sea turtles of the
coast of the United States is shrimp trawling. Other important factors include other
fisheries and entanglement in lost fishing gear and marine debris, dredging, collisions with
boats, petroleum-platform removal, power plant intake pipes, direct take, pollution,
ingestion of plastics, and
disease (NAS, 1990).
We discuss each of these
factors briefly below.
Shrimp fishing. In
the absence of "turtle-
excluding" devises,
shrimp fisheries take a
large number of sea
turtles incidental to their
capture of shrimp, and
this may represent the
largest single source of
adult sea turtle mortality
(NAS, 1990). Although
the National Marine
Fishery Service originally
estimated that 11,000
turtles are killed each year by shrimpers, a special panel of the National Academy of
Sciences (NAS) estimated that shrimp boats working the United States' southern Atlantic
coast and Gulf of Mexico may have been killing up to four times that level (NAS, 1990;
Abramson, 1990*P). Murphy and Hopkins-Murphy (1989) found that 83 percent of the
78 studies they reviewed suggested that shrimp trawling is a major source of sea turtle
mortality. Several investigators have documented increased incidence of dead turtles on
beaches with the onset and peak of shrimp trawling activities (Hellestad, et al. 1982;
other studies summarized by Caillouet et al., 1991). Loggerhead populations are
declining in areas where there is active shrimp fishing (e.g., Georgia and South Carolina;
Murphy and Hopkins-Murphy, 1989; NAS, 1990), but may be increasing where shrimp
fishing is absent or low (e.g., southern Florida) (NAS, 1990). NAS (1990) estimated that
70 to 90 percent of the turtles washed up on shore during periods when fisheries are
open in South Carolina and Texas are killed in shrimp trawls.
The NAS panel concluded that use of nets with escape doors could reduce sea
turtle drownings by 97 percent (Abramson, 1990*P). Regulations requiring the use of
;
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turtle-safe nets were first issued in 1987, but the regulations were contested and not
strictly enforced. The NAS findings will support Federal efforts to enforce the
regulations.
Otfier fisheries and discarded or lost gear. Data on the association of turtle
mortality with other fisheries and entanglement in gear are sporadic and thus difficult to
assess. NAS (1990) cited numerous reports from different regions that sea turtles have
become entangled in fin fish trawls, seines, pompanon gill nets, weirs, traps, long lines,
lost fishing gear, and other debris.
Dredging. In the United States, there were at least 149 confirmed incidents in
which sea turtles were entrained by hopper dredges working in two shipping channels
from 1980 to 1990 (NAS, 1990). The majority of the turtles found were dead or dying.
Collisions with boats. In the United States, many sea turtle deaths (50 to 500
loggerhead and 5 to 50 Kemp's ridley turtles) and strandings have been associated with
collisions with boats. Areas with high concentrations of recreational boat traffic are of
most concern (NAS, 1990).
Petroleum-platform removal. The use of explosives when removing petroleum
platforms has likely caused the mortality of numerous sea turtles (50 to 500 loggerhead
and 5 to 50 Kemp's ridley turtles) and other large marine organisms (NAS, 1990).
Power plant intake pipes. Numerous sea turtles (about 50 per year) have been
found dead in the intake pipes for cooling water at coastal power plants of the United
States. One power plant where the incidence has been high (averaging 11 turtle deaths
per year) is located where the continental shelf along their migratory route is narrow,
forcing sea turtles to pass close to the shore (NAS, 1990).
Direct take. The extent of this problem is unknown. Some illegal take of turtles
occurs in the United States, but the numbers are probably negligible (NAS, 1990). In
Mexico, on the other hand, Aridjis (president of a Mexican environmental organization)
has stated that 75,000 endangered sea turtles were killed by fisherman in 1989 alone,
most of which are sold to Japan (Branigin, 1990*P). Recently, with pressure from the
United States, Japan has agreed to end importation of hawksbill turtles (Abramson,
1991*P).
Pollution. Few studies have assessed the potential or actual impacts of pollution
on sea turtles; thus, the effects of pollution cannot be estimated. Tissues and eggs have
been found to be contaminated with organochlorines, heavy metals, hydrocarbons, and
radionuclides, however (NAS, 1990). An increased incidence of disease, at least in one
location, is suspected of being associated with marine pollution (see below).
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Disease. Cutaneous fibropapillomatosis, a disease of green turtles, has been,
reported with increasing frequency in Florida (Witherington and Ehrhart, 1989; as cited
in NAS 1990) and the Hawaiian Islands (Balazs, 1986; as cited in NAS, 1990). In
addition, unconfirmed cases have been reported from Puerto Rico, Curacao, Venezuela,
and Belize (E.H. Williams, pers. comm.). In Florida's Indian River, up to 52 percent of
the green turtles have fibropapillomas (tumors that grow on both the inside and the
outside of the turtle's skin). Research on the cause of the disease is in progress
(Jacobson et al., 1989), and there is concern that ocean pollution may be at least partly
responsible (Reuter, 1990*P).
Ingestion of plastic. An estimated 100,000 marine animals, including sea turtles, die
each year from eating or becoming entangled in plastic debris in the ocean.
Approximately 24,000 metric tons of plastic packaging is dumped into the ocean each
year. National Marine Fisheries Service (NMFS) scientists estimated that one-third to
one-half of all turtles have ingested plastic products or byproducts (Cottingham, 1988; as
cited in NAS, 1990). Carr (1987) discussed the implications of a recent discovery that
juveniles of many species of sea turtles may spend three to five years feeding and
swimming near the surface of the open-ocean (i.e., pelagic stage). During this time, they
depend for food on oceanic convergences (e.g., fronts, rips, and driftlines).
Unfortunately, these same convergences concentrate buoyant ocean debris (e.g., plastic
bags, styrofoam beads, and tar balls) which the turtles can mistake for food. The
leatherback and the olive ridley appear to be mainly surface foragers after reaching
maturity, and so may remain vulnerable to surface ocean debris as adults. Other species
for which the surface feeding stage ends just prior to sexual maturity, no longer face this
threat (i.e., the animals become benthic foragers in coastal areas). Juvenile loggerheads
containing tar pellets and plastic beads have been found in great numbers washed up on ;
the Florida east coast. Some researchers believe that the marked tendency of
leatherbacks to ingest sheets and bags of plastic film results from the plastic sheets'
resemblance to jellyfish (Carr, 1987).
2.6.3. Continued Monitoring
Numerous organizations monitor specific populations of turtles. These include the
American Museum of Natural History, World Wildlife Fund, Center for Marine
Conservation, the World Conservation Union, the Durrell Institute of Conservation and
Ecology in Canterbury, England, and the newly established Marine Ecological
Disturbance Information Center (MEDIC) in Puerto Rico (see Section 2.7).
United States government agencies that monitor several species of turtle include
the Department of the Interior, Fish and Wildlife Service and the National Marine
Fisheries Service of the National Oceanic and Atmospheric Administration.
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Witherington, BE, and Bjorndal, KA. 1991. Influences of artificial lighting on the
seaward orientation of hatchling loggerhead turtles Caretta caretta. Biol. Conserv.
55:139-149.
2.6.5. Popular Press Bibliography
Abramson, R. 1990. Shrimp boats kill 44,000 turtles, scientists say. Los Angeles Times.
May 18, 1990, vol 109, col 1, p A20.
Abramson, R. 1991. Japan yields to US pressure, will halt trade in endangered turtles.
Los Angeles Times. May 18, 1991, vol 110, col 1, p A10.
Branigin, W. 1990. Imperiled turtles slaughtered in Mexico: Environmentalists say
skinners, egg poachers could end species. Washington Post. February 18, 1990, p A44.
Burdick, L. 1989. Sea turtles swim for survival: On the world's beaches, the giant
reptiles return to nest - but in ever smaller numbers. Christian Science Monitor. August
29, 1989, vol 81, No. 192, col 1, p 12.
Bury, RB. (ed.) 1982. North American tortoises: Conservation and ecology.
Washington, DC: Wildlife Research Report 12.
Dean, C. 1992. Their beaches eroding, threatened sea turtles have few places to nest.
New York Times. March 17, p C4.
Elegant, S. 1991. The plight of Malaysia's leatherback; out of control tourists are
endangering turtles at egg-laying sites on the Rantau Abang beach. New York Times.
May 19, 1991, sect 5.
Lancaster, J. 1990. Study blames shrimpers for sea turtle deaths. Washington Post.
May 20, 1990, p A10.
NYT. 1989. US acts on sea turtles. New York Times. August 8, 1989, vol 138, col 3, p.
C5(L).
PR. 1990. The Mojave desert tortoise is no ninja, but it has stopped some big Las
Vegas developers dead in their tracks. People Weekly (May 21).
Reuter. 1990. Makeshift Florida lab studies tumors afflicting sea turtles. Washington
Post. August 29, 1990.
Stevens, WK. 1990. Big effort is begun to reverse decline of turtles. New York Times.
March 13, 1990, vol 139, col 1, pp B7, C4.
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WSJ. 1991. Japan bans by '93 imports of endangered sea turtles. (Japan protects turtles
to avoid US trade sanctions). Wall Street Journal. June 20, 1991, p A10.
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2.7. Marine Mammals
Recent mass mortalities of bottlenose dolphins in the United States (1987 and
1990) and striped dolphins in the Mediterranean (1991) have triggered public and
scientific concern that pollution, in addition to incidental catches of dolphins by the tuna
fishing industry, may threaten dolphin populations. Pathological examination of dolphins
stranded in the United States in 1987 suggest a chronic immune system suppression.
This could have been a consequence of sublethal exposure to a red tide and/or a
consequence of unusually high concentrations of PCBs in the dolphin tissues.
In addition, recent "epidemics" of a distemper-like virus have caused mass
mortalities among several populations of seals. Some suspect that coastal pollution has
increased the seals' susceptibility to the virus, but the cause of the outbreaks is as yet
undetermined. Unusually warm temperatures also may contribute to outbreaks of the
virus.
In addition to mass mortality events, many pinniped (i.e., seals, sea lions, and
walruses) populations have been declining recently. Bioaccumulation of PCBs or other
toxic substances are known to reduce reproductive success in seals, and may be
contributing to these population declines in some areas.
Because of their position high in the marine food chain and because they use body
fat for insulation, both groups of marine mammals are particularly susceptible to
chemicals that bioaccumulate in fatty tissues (e.g., PCBs). As a result, these groups
might serve as sensitive monitors of marine pollution. The causes of mass mortalities
and population declines in these groups therefore appears to warrant additional
investigation. We review the dolphin and pinniped trends separately in Sections 2.7.1
and 2.7.2, respectively.
2.7.1. Dolphins
2.7.1.1. Description
Background. Dolphins are piscivorous (i.e., fish eating), and their position high in
the food chain makes them especially susceptible to bioaccumulating higher levels of
certain chemicals (e.g., PCBs, mercury) than other marine species, particularly in their
fat. At times of stress, dolphins mobilize their fat reserves, which might suddenly release
accumulated contaminants to their blood.
Trends, Bottlenose dolphin die-offs in the North Atlantic occurred in 1987 and
1990. During an 11-month period beginning in the summer of 1987, an estimated 3,000
bottlenose dolphins (approximately half of the Atlantic coast dolphin population) died
along the Atlantic coast of the United States (Scott et al., 1988), of which over 740 were
found stranded (Geraci, 1989; McKay, 1989). The stranded dolphins exhibited skin
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lesions and internal lesions characterized by fibrosis (indicating a chronic infection) in the
lung, liver, pancreas, and heart (Geraci, 1989). Systemic bacterial infection appeared to
be the ultimate cause of death (Geraci, 1989). Since January of 1990, more than 300
dead or dying bottlenose dolphins, more than twice the usually expected number for the
time period, have washed ashore along the Gulf states, (Lancaster, 1990*P). The
National Marine Fisheries Service is investigating the cause of the 1990 strandings.
In 1990, at least 1,000 striped dolphins washed up on the Mediterranean coastlines
of Spain, Italy, and France (Jones, 1990; Simons, 1992*P), and in late 1991, hundreds of
dead and dying striped dolphins were found beached on the coast of Italy, Sicily, and a
Greek island (Jones, 1991b; Simons, 1992*P).
2.7.1.2. Hypotheses
Hypotheses to account for the recent dolphin die-offs include poisoning by a
naturally occurring red tide, infection following immunosuppression resulting from the
accumulation of toxic substances, and natural occurrences. These are discussed below.
Red tide. Geraci (1989) concluded that the most likely cause of the 1987
bottlenose die-off was poisoning by a "red tide" algal bloom. Red tide algae occur
naturally and produce brevetoxin, a potent toxin of the nervous system. Eight of 17 (i.e.,
47 percent) dolphins analyzed in the 1987 killing contained this neurotoxin; the other 9
did not contain detectable levels. Geraci (1989) hypothesized that the toxin made the
dolphins susceptible to the numerous chronic disorders that finally killed them. The
results of this report remain controversial, however (Lancaster, 1990*P; McKay, 1989).
For example, brevetoxin is not known to weaken the immune system of organisms, and
the kind of red tide that produces brevetoxin is common in the Gulf of Mexico, where no
die-offs had been reported as of 1989 (McKay, 1989). In the Mediterranean striped
dolphin deaths, red tides were ruled out because none of the dolphins examined showed
signs of algal toxins (Jones, 1990).
Pollution-impaired immune system. Toxic chemicals might have weakened the
immune system of the dolphins, thus increasing their susceptibility to disease (McKay
1989). Geraci (1989) reported high levels of PCBs, DDT, and chlordane in the
bottlenose dolphins stranded in 1987. Levels of PCBs were, on average, an order of
magnitude higher than in other cetaceans, and several dolphins had the highest PCB
tissue levels on record (compared with the reports of Gaskin et.al., 1971, 1983; Aguilar,
1983; Tanabe et al., 1984; Martineau et al., 1987; Muir et al. 1988; as cited in Geraci,
1989). Further analysis of PCB levels in the bottlenose dolphins collected in the 1987/88
mass mortality event and in two other species that were not affected (i.e., common and
white-sided dolphins caught incidentally in fishing nets) indicated higher levels in the
bottlenose dolphins (Kuehl et al., 1991). Furthermore, the bottlenose dolphins were
found to be contaminated with other yet unidentified polychlorinated and polybrominated
chemicals (Kuehl et al., 1991).
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PCBs are known immunosuppressants (Safe, 1984; Smailowicz et al., 1989;
Thomas and Hinsdill, 1978; Tryphonas et al., 1989). Greenpeace noted that PCBs are
known to cause lesions such as those found on many dolphins in 1987 (McKay, 1989).
Geraci (1989) did not believe that contaminants could be the major cause of the event,
however, because there are vast differences in response to these compounds within and
between species, and the timing of the outbreak did not coincide with any major release
of contaminants. McKay (1989) observed that contaminants may have killed some
animals directly or weakened them, making them susceptible to disease, infection, and
other causes of mortality. The rather sudden nature of the die-off may have resulted
from a "triggering" stress or lack of food that caused the dolphins to rely more heavily
than usual upon their fat reserves for energy.
In the case of the European striped dolphin deaths, researchers at the University
of Barcelona found PCBs in some animals at levels up to 10 to 50 times levels that are
considered dangerous for humans (Simons, 1992). It is not known whether this could
have increased their susceptibility to the virus that appears to have caused their deaths
(Jones, 1990).
Disease. Many of the dolphins analyzed in the 1987 die-off had bacterial and viral
infections which may have killed the animals. However, the "pattern of illness that could
be associated with a known pathogen" does not support the hypothesis that disease was
the ultimate cause of the massive mortality of dolphins (Geraci, 1989).
The majority of the Mediterranean striped dolphin deaths, however, were
attributed to a morbillivirus (Jones, 1990). A different strain of morbillivirus was
responsible for the western Mediterranean die-off in 1990 than for the eastern
Mediterranean die-off in late 1991. There are no records in the literature over the past
hundred years of a cluster of virulent epidemics in dolphins like the ones observed in the
Mediterranean (S. Kennedy, as reported by Simons, 1992*P). The possibility that PCB's
or other toxic substances may have acted as an immunosuppressant is under
consideration (Jones, 1990; Simons, 1992*P).
2.7.2. Pinnipeds (Seals, Sea Lions, and Walruses)
2.7.2.1 Description
Background. Pinnipeds live mainly in the far north and extreme south, many
species congregating in dense aggregations on "haul-outs" along coastal areas during the
mating and pupping season. Like dolphins, the position of seals, sea lions, and walruses
near the top of the marine food chain makes them especially susceptible to
bioaccumulating higher levels of certain chemicals (e.g., PCBs, mercury), particularly in
their blubber (Addison, 1989). These contaminants can be released relatively quickly
when the animal mobilizes its reserves of fat at times of stress, such as during lactation or
when it molts (Harwood and Reijnders, 1988).
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Trends. In recent
decades, populations of
several species of
pinnipeds in the United
States have exhibited
population declines
despite substantial relief
from hunting pressures
afforded by the Marine
Mammal Protection Act
of 1972 (MMPA). In
addition, mass
mortalities and
population declines of
seals around the
northern hemisphere
have captivated public
attention (Dickson, 1988;
Dietz et al., 1989;
Harwood, 1989, 1990a,b;
Stirrup, 1990;
Stolzenburg, 1990).
Examples of mass mortalities and continuing population declines are presented in
Exhibits 2.7.1 and 2.7.2, respectively.
2.7.2.1. Hypotheses
In the early part of this century, hunting was responsible for decimating many
pinniped populations in the Northern hemisphere to a few percent of their original
nineteenth century numbers (e.g., Durant and Harwood, 1986; Helander and Sjoasen,
1985).12 Since passage of the MMPA in the United States, other threats have
emerged, including coastal development, habitat destruction, marine pollution,
interactions with fisheries, and entanglement in marine debris and fishing nets (WRI,
1988). The mass mortalities of seals in several areas of the North Atlantic have been
diagnosed as due to phocid distempervirus (PDV) and secondary pulmonary and other
infections (Osterhaus and Vedder, 1989). The cause(s) of the recent outbreaks of PDV
are not clear, and some investigators have suggested that pollution-impaired immune
defenses may be responsible. Warmer than usual ocean temperatures also may play a
role. We discuss the hypotheses to explain mass mortalities and continued population
declines separately below.
12 Illustration of northern fur seal in the box reproduced with permission of the artist, Kimberly Hall:
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Exhibit 2.7.1. Mass mortalities of pinnipeds.
1955: In the Antarctic, over 3,000 crabeater seals (Lobodon carcinophagus)
died; no live pups were found, and mortality was estimated at 85% (da
Dilva et aL, 1957; Laws and Taylor, 1957).
1978: 1,200 walruses (Odobenus rosmarus) out of a herd of around 6,000
died in the Bering Strait, apparently from physical trauma (e.g., trampling
by other walruses) (Fay and Kelly, 1980).
1979-1980: At least 500 harbor seals (Phoca vitulina) out of a population
of 10 to 14 thousand died along the coast of New England from an
influenza A type virus (Geraci et al., 1982).
1987: In the fall, several thousand Baikal seals (Phoca sibirica) out of a
population of up to 100,000 died in the Soviet Union (Grachev et al.,
1989).
1988: At least 17,000 to 18,000 European harbor seals died in several
areas, e.g., Kattegat, Wadden Sea, Skagerrak, Limfjorden, western Baltic,
Norway, and the British Isles (Dietz et al., 1989; Osterhaus et al., 1990)
The die-off was preceded by a few months by increased rates of abortion
(Dietz et al., 1989). In some areas, 90% of the local population of seals
died in 40 to 60 days. The primary cause of death was acute and severe
bacterial pneumonia.
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Exhibit 2.7.2. Declining populations of pinnipeds.
The population of Stellar's sea lion (Eumetopias jubatus) in the eastern
Aleutian Islands and the Gulf of Alaska decreased 90% from 50,000 at the
beginning of the 1960's to 5,000 by the late 1960's (Stirrup, 1990). The
population continues to decrease at a rate of 5 to 7% per year (Braham et
al., 1980; Merrick et al., 1987; Calkins and Goodwin, 1988; as cited in
Pitcher, 1990).
Gulf of Alaska harbor seals (Phoca vitulina richardsi) at Tugidak Island
have declined by about 85% between 1976 and 1988 (Pitcher, 1990).
The decline of northern fur seals (Callorhinus ursinus) in the Pribilof
Islands at an annual rate of 7.5% in the late 1970's may have stabilized in
the 1980s (Fowler, 1982, 1985; York and Kozloff, 1987; as cited in Pitcher
1990).
Southern Dutch harbor seals (Phoca vitulina) in the Delta area of the
Wadden Sea declined from 1,000 to 10 or 20 seals between 1955 and 1969,
and are now extinct (Reijinders, 1985).
Northern Baltic grey seals (Halichoerus grypus) and ringed seals (Pusa
hispida) continued to decline in the 1970's despite reduced hunting pressure
(Hook and Johnels, 1972; as cited in Addison, 1989).
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Mass Mortalities
PDV (phocid distempervirus). Little doubt remains that the proximate cause of the
recent mass mortalities of harbor seals (Exhibit 2.7.1) was an infectious disease outbreak
with a morbillivirus (Phocid distempervirus-PDV) closely related to canine distemper virus
(CDV) (Hofmeister et al, 1988; Osterhaus and Vedder, 1989; Osterhaus, 1989;
Osterhaus et al., 1988, 1990; Kennedy et al., 1988; Mahy et al., 1988; Cosby et al., 1988;
as cited in Law et al., 1989).13 CDV is known to depress the immune system in dogs
(Appel, 1987; as cited in Osterhaus and Vedder, 1989), and PDV is likely to have
immunosuppressive effects in seals (Osterhaus and Vedder, 1989). The majority of
deaths occurred as a result of secondary bacterial infections rather than due to PDV
directly (Harwood, 1990a; Osterhaus and Vedder, 1989).
It is not clear whether the recent outbreaks of PDV are the result of
anthropogenic stresses on these populations or naturally occurring phenomena. Mass
mortalities of various North Atlantic seal populations showing pneumonia-like symptoms
have been reported at intervals of about 50 years throughout the 1800 and 1900's
(Harwood, 1990b; Dietz et al., 1989). Nonetheless, there is evidence supporting the roles
of pollution and ocean warming events as contributing factors to the outbreak, as
discussed below.
Pollution-impaired immune system. Moderate to high levels of various
pollutants have been detected in pinnipeds, particularly several populations of
European seals, since the late 1960's. These include PCBs (Anas, 1974; Duinker
et al., 1979; Law et al. 1989), DDT/DDEs (Anas, 1974; Duinker et al., 1979; Law
et al., 1989), chlordane compounds (Kerkhoff et al., 1981; Kerkhoff and de Boer,
1982), and mercury (Duinker et al., 1979). PCBs are known to depress immune
function in rats (Safe, 1984; Smailowicz et al., 1989; Thomas and Hinsdill, 1978;
Tryphonas et al., 1989) and possibly to reduce plasma concentrations of retinol
(i.e., vitamin A) and thyroid hormone, which might result in increased
susceptibility to microbial infections (Brouwer et al., 1989). Some investigators
report that the disease outbreaks are more severe in seal populations inhabiting
more polluted coastal areas (Duinker et al., 1979; Harwood, 1990a). Other
evidence suggests, however, that pollution may have played only a small role. For
example, the majority of the seals found dead in England contained concentrations
of PCB, DDT, HCB, and HCH at the lower end to middle of the spectrum of
contamination levels observed in the North and Baltic seas (Law et al., 1989).
Moreover, Harwood and Reijnders (1988) observed that the greatest number of
seal deaths had not occurred in the most polluted areas of the Wadden and Baltic
13A11 of Koch's postulates for cause-and-effect have been satisfied, including virus isolation and
characterization and protection of seronegative seals against fatal-challenge infection by vaccination with
inactivated CDV vaccines (Osterhaus and Vedder, 1989; Wickelgren, 1989).
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Seas. A quantitative study of the relationship between measured environmental
contaminant levels and seal mortality incidence has not yet been conducted.
Global warming or short-term temperature fluctuations. Lavigne and Schmitz
(1990) have examined records of regional air temperatures and found that
preceding each of five major seal die-offs, mean air temperatures were 1 °C to 3
°C higher than the preceding 10-year average.
In summary, the cause of the outbreaks of PDV in seal populations in recent
years is unknown, and it is not clear whether the outbreaks reflect naturally occurring
phenomena or result from one or more human-caused stresses.
Declining Populations
Pollution-impaired reproduction. In general, seals in the waters of Japan, the
United States, other north Pacific countries, and in Europe have been found to be
contaminated with organochlorines and metals to varying degrees, although most at
apparently nontoxic levels (Himeno et al., 1989; Duinker et al., 1979). High tissue
concentrations (i.e., parts per million and above) of several chemical compounds,
particularly PCBs and DDT/DDEs, have been measured in seal blubber since the 1960's
(Anas, 1974; Duinker et al., 1979; Law et al., 1989; Reijnders, 1980, 1985; Shaw, 1971).
Several studies suggest that these high contaminant levels have caused the reduced
reproductive success observed in several seal populations (Dietz et al., 1989; Hook and
Johnels, 1972; Jensen et al., 1969; Koeman et al., 1972 as cited by Reijnders, 1985;
Reijnders 1976, 1978, 1980, 1981b, 1986; Law et al., 1989). Analyses by Helle et al.
(1976a,b) and Addison (1989) have suggested that in ringed seals, PCB blubber lipid
concentrations over about 70 ppm (and/or higher DDT/DDE concentrations) are
associated with reproductive defects caused by uterine occlusions. Whether the high
organochlorine residues cause these effects, or whether reduced reproductive success isa
parallel result of some other cause is hot yet clear (Addison, 1989).
Additional evidence that contaminant-induced reproductive effects can cause
population declines comes from the Dutch Wadden Sea, where the Rhine River has
delivered high loads of PCBs and other pollutants over the past several decades. The
local population of common seals crashed from 3,000 in 1950 to fewer than 500 in 1975
(Duinker et al., 1979). Reduced reproductive success appears to be the cause, and
concentrations of PCB, DDT, copper, lead, zinc, and cadmium in tissue samples from
seals found dead in the Dutch Wadden were higher than in those from a stable
population in the German Wadden Sea (Duinker et al., 1979). Reijnders (1986)
experimentally demonstrated that a diet of fish from the Dutch Wadden Sea could
reduce reproductive success in seals. Seals fed Dutch Wadden Sea fish, containing doses
of 1.5 mg PCB/day and 0.22 mg DDE/day for two years, experienced significantly reduced
reproductive success compared with a "control group" fed northeastern Atlantic fish and
receiving doses of 0.4 mg PCB/day and 0.13 mg DDE/day. The effect appears to occur
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in the post-ovulation phase, with the period around implantation being most sensitive.
The effect is reversible; after changing the diet of the experimental group to fish from
the northeast Atlantic, the reproductive success of the experimental group returned to
control levels (Reijnders, 1986).
Some infectious agents (e.g., Leptospira sp.} have been found to interfere with
reproduction, and this effect may be magnified if the animals are already immune-
deficient as a result of poisoning with organochlorine pollutants (Risebrough et al., 1980).
Marine debris. Fowler (1982, 1987) has suggested that the recent decline in
abundance of northern fur seals in the Pacific is the result of excess mortality caused by
entanglement in marine debris. The abundance of debris, principally net fragments, in
the areas occupied by fur seals, and the number of observed entanglements support the
hypothesis. With harbor seals or Steller sea lions, however, investigators have found no
evidence that entanglement is a serious problem (Stewart and Yochem, 1985; Merrick et
al., 1987; as cited in Pitcher 1990).
Reduced food supply. Some investigators believe that the decline of the Stellar sea
lion (Exhibit 2.7.2) may be the result of overfishing in the Shelikof Strait, which reduces
the size and nutritional value of the sea lion's food supply (Stirrup, 1990). Definitive
evidence is still lacking, however.
Unknown. The North Atlantic populations of harbor seals, Steller sea lions, and
northern fur seals have exhibited similar patterns of decline over time, and yet a single
causative agent that the three populations have in common has not yet been identified
(Pitcher, 1990).
2.73. Continued Monitoring
Several United States organizations have been involved in investigating mass
mortalities in marine mammals, including the National Marine Fisheries Service (NMFS)
of the National Oceanic and Atmospheric Administration (NOAA), the Southeastern US
Marine Mammal Stranding Network, Texas A&M University, and the Armed Forces
Institute of Pathology. Various organizations track marine mammals in Europe and
elsewhere as well.
The Marine Ecological Disturbance Information Center (MEDIC), recently
established at the Department of Marine Sciences at the University of Puerto Rico (P.O.
Box 908, Lajas, PR 00667), is serving as a communication hub for information concerning
not only coral reef bleaching events (see Section 2.7), but other major marine
disturbances and may assist tracking mass mortalities of marine mammals in the future.
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2.7.4. References
Dolphins
Aguilar, A. 1983. Organochlorine pollution in sperm whales, Physeter macrocephalus,
from the temperate waters of the Eastern North Atlantic. Mar. Poll. Bull. 14:349-352.
Gaskin, DE, Holdrinet, M, and Frank, R. 1971. Organochlorine pesticide residues in
harbor porpoises from the Bay of Fundy region. Nature 233:499-500.
Gaskin, DE, Frank, R, and Holdrinet, M. 1983. Polychlorinated biphenyls in harbour
porpoises, Phocoena phocoena (L), from the Bay of Fundy, Canada and adjacent waters,
with some information on chlordane and hexachlorobenzene levels. Arch. Environ.
Contam. Toxicol. 12:211-219.
Geraci, JR (Principal Investigator). 1989. Clinical investigation of the 1987-1988 mass
mortality of bottlenose dolphins along the US central and south Atlantic coast. Final
Report to National Marine Fisheries Service, US Navy, Office of Naval Research, and
Marine Mammal Commission.
Jones, P. 1990. Mediterranean dolphin deaths. Mar. Poll. Bull. 21:501.
Jones, P. 1991a. What caused dolphin deaths? Mar. Poll. Bull. 22:317.
Jones, P. 1991b. Dolphin epidemic spreads. Mar. Poll. Bull. 22:576.
Kuehl, DW, Haebler, R, and Potter, C. 1991. Chemical residues in dolphins from the
US Atlantic coast including Atlantic bottlenose obtained during the 1987/88 mass
mortality. Chemosphere 22:1071-1084.
Martineau, D, Beland, P, and Desjardins, C, et al. 1987. Levels of Organochlorine
chemicals in tissues of beluga whales (Delphinapterus leucas) from the St. Lawrence
Estuary, Quebec, Canada. Arch. Environ. Contam. Toxicol. 16:137-147.
Muir, DC, Wagemann, R, and Grift, NP, et al. 1988. Organochlorine chemical and
heavy metal contaminants in white-beaked dolphins (Lagenorhynchus albirostris) and pilot
whales (Globicephala melaena) from the coast of Newfoundland, Canada. Arch. Environ.
Contam. Toxicol. 17:613-629.
Safe, S. 1984. Polychlorinated biphenyls (PCBs) and polybrominated biphenyls (PBBs):
Biochemistry, toxicology, and mechanisms of action. CRC Crit. Rev. Toxicol 13: 319-395.
Scott, GP, Burn, DM, and Hansen, LJ. 1988. The dolphin dieoff: Long-term effects
and recovery of the population. In: Proc. Oceans '88, Baltimore, MD. Pp. 819-823.
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Smailowicz, RJ, Andrews, JE, and Riddle, MM, et al. 1989. Evaluation of the
immunotoxicity of low level PCB exposure in the rat. Toxicology 56:197-211.
Tanabe, S, Tanaka, H, and Tatsukawa, R. 1984. Polychlorobiphenyls, total-DDT, and
hexachlorocyclohexane isomers in the western North Pacific ecosystem. Arch. Environ.
Contam. Toxicol. 13:731-738.
Thomas, PT, and Hinsdill, RD. 1978. Effect of polychlorinated biphenyls on the
immune responses of rhesus monkeys and mice. Toxicol. Appl. Pharmacol. 44:41-51.
Tryphonas, H, Hayward, S, and ,0'Grady, L, et al. 1989. Immunotoxicity studies of PCB
(Aroclor 1254) in the adult rhesus (Macaco, mulatto) monkey—preliminary report. Int. J.
Immunopharmacol. 11:199-206.
Pinnipeds
Addison, RF. 1989. Organochlorines and marine mammal reproduction. Can. J. Fish.
Aquat Sci. 46:360-368.
Anas, RE. 1974. DDT plus PCB's in blubber of harbor seals. Pestic. Monit. J. 8:12-14.
Appel, MJ. 1987. Canine distemper virus. In: Virus infections of vertebrates, vol. I:
Virus infections of carnivores. Amsterdam: Elsevier Scientific Publ. Co.
Braham, HW, Everitt, RD, and Rugh, DJ. 1980. Northern sea lion population decline in
the eastern Aleutian Islands. J. Wildl. Manage. 44:25-33.
Brouwer, A, Reijnders, PJ, and Koeman, JH. 1989. Polychlorinated biphenyl
(PCB)-contaminated fish induces vitamin A and thyroid hormone deficiency in the
common seal (Phoca vitulina). Aquat. Toxicol. (Amst.) 15:99-106.
Calkins, D, and Goodwin, E. 1988 (unpubl.). Investigation of the declining sea lion
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Cosby, SL, McQuaid, S, and Duffy, N, et al. 1988. Characterization of a seal
morbillivirus. Nature (London) 336:115-116.
da Dilva, J, Laws, RM, and Taylor, RJ. 1957. A mass dying of crabeater seal, Lobodon
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Dickson, D. 1988. Canine distemper may be killing North Sea seals. Science 241:1284.
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Duinker, JC, Hillebrand, MT, and Nolting, RF. 1979. Organochlorines and metals in
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Durant, S, and Harwood, J. 1986. The effects of hunting on ringed seals (Phoca hispida)
in the Baltic. I.C.E.S. C.M. 10.
Fay, FH, and Kelly, BP. 1980. Mass natural mortality of walruses (Odobenus rosmarus)
at St. Lawrence Island, Bering Sea, Autumn 1978. Arctic 33:226-245.
Fowler, CW. 1982. Interactions of northern fur seals and commercial fisheries. Trans.
N. Am. Wildl. Conf. 47:278-292.
Fowler, CW. 1985. Status review: Northern fur seals (Callorhinus ursinus) of the
Pribilof Islands, Alaska. Tokyo, Japan: Background paper submitted to the 28th Annual
Meeting of the Standing Scientific Subcommittee of the North Pacific Fur Seal
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Fowler, CW. 1987. Marine debris and northern fur seals: A case study. Mar. Pollut.
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Geraci, JR, St. Aubin, DJ, and Barker, IK, et al. 1982. Mass mortality of harbor seals:
Pneumonia associated with influenza A virus. Science 215:1129-1131.
Grachev, MA, Kumarev, VP, and Mamarev, LV, et al. 1989. Distempervirus in Baikal
seals. Nature 338:209.
Harwood, JH. 1989. Lessons from the seal epidemic. New Scientist 121:38-42.
Harwood, JH. 1990a. What have we learned from the 1988 seal epidemic? Biologist
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Harwood, JH. 1990b. Mass mortality in marine mammals: Its implications for
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Harwood, JH, and Reijnders, PJ. 1988. Seals, sense and sensibility. New Scientist
120:28-29.
Helander, B, and Sjoasen, T. 1985. Salbestanden vid svenska syd- och ostkusten
1975-1984. Stockholm, Sweden: Naturhistoriska Riksmuseet. Salinformation 1985: 2.
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Helle, E, Olsson, M, and Jensen, S. 1976a. DDT and PCB levels and reproduction in
ringed seal from the Bothnian Bay. Ambio 5:188-189.
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117
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118
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2.7.5 Popular Press Bibliography
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February 11, 1990, p A2. ,
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2.8. Forests Worldwide
Summary. Forests are declining and being damaged worldwide. In the tropics,
clearing land for agriculture and other land uses is the most significant problem, whereas
in the north temperate zone, forest dieback resulting from atmospheric pollution is an
additional problem.
Clearing of tropical rainforest is proceeding at an unprecedented rate that could
result in the complete loss of such forests by the year 2050. In North America,
deforestation and reforestation are more balanced; however, old growth forests are at
risk of being lost completely in the Pacific Northwest.
Beyond the conclusion that general atmospheric pollution is leading to forest
dieback in the developed countries, researchers have not been able to identify a more
specific common cause across the continents. Because multiple pollutants are generally
present in the forests of concern, attribution of forest dieback to specific direct or
indirect effects of acid rain, ozone, or other atmospheric sources of pollution remains
somewhat controversial. Current evidence implicates a variety of natural biotic and
abiotic stresses upon which are superimposed physical and chemical stresses of
anthropogenic origin that may have originated long distances from the affected sites.
Tropical and temperate deforestation and temperate forest dieback are discussed
in Sections 2.8.1 and 2.8.2, respectively.
2.8.1. Deforestation
2.8.1.1. Description
Background. Closed forests cover approximately 2.8 billion hectares, or 21 percent
of the Earth's land surface (WRI, 1988). Of the closed forests, 43 percent are found in
the tropics and 57 percent are in the temperate zone (WRI, 1988). Tropical moist
forests occupy just over one billion hectares and constitute 90 percent of all tropical
closed forests (the remainder being deciduous or semideciduous). Tropical rain forests
account for about 66 percent of all tropical forests. Of the closed forests, 62 percent are
broadleaf and 38 percent are coniferous. Developed nations contain over 90 percent of
all coniferous forests and developing nations 75 percent of all broadleaf (i.e., hardwood)
forests (WRI, 1988).
Trends. Tropical deforestation is proceeding at an annual rate of 40 million to 50
million acres, an area the size of the state of Washington (Shabecoff, 1990*P; AP,
1990*P). This estimate, based on 1987 remote sensing data from the National Oceanic
and Atmospheric Administration and Landsat satellites, is 50 to 80 percent higher than
previously thought, based on 1980 data (WRI, 1990; Houghton, 1990; Shabecoff, 1990*P).
The majority of the increase in deforestation rate is occurring in tropical America rather
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than in tropical Africa or Asia (Houghton, 1990). Brazil is losing between 12.5 and 22.5
million acres each year; India is losing 3.7 million acres and Indonesia 2.2 million acres
per year (Myers, 1989). Nine key countries alone account for more than 29 million acres
of the estimated loss per year (WRI, 1990).14 At this rate, tropical moist forests would
be completely cleared in 50 to 60 years (assuming 2,700 million acres remaining; WRI,
1988). North temperate forests already have been reduced dramatically by land
clearing of the past. A reverse of this trend is evident in the eastern United States where
many agricultural lands have been allowed to revert to forest (Exhibit 2.8.1).
Continued loss of old growth forests and north temperate rain forests is also of
concern in the United States and Canada. For example, as of 1988, the Wilderness
Society estimated that only 141,000 acres of continuous tracts (i.e., further than 400 feet
from clearcuts or road) of old growth forest exists in the Pacific Northwest (Morrison,
1988). By 1987, the timber industry was logging an estimated 170 acres of old growth
every day (WS, 1988). At this rate, all old-growth forest in the Pacific Northwest would
be eliminated in 2.3 years. Recently, concern is mounting that northeastern forests in the
United States may be at risk of extensive development.
The rapid loss of tropical forests and temperate latitude old growth forests are
particularly alarming because of the relationship of forests to other organisms, including
species also threatened by other aspects of man's activities. Slash and burn deforestation
accounts for about 33 percent fo the annual emissions of carbon dioxide (a greenhouse
gas that can contribute to global warming) caused by humans (WRI, 199). Forests are
responsible for the habitat needed by the neotropical migrants, amphibians, fish, and
other organisms. Living forests absorb carbon dioxide, thereby helping to offset the
increasing levels of greenhouse gases contributing to possible global warming. Locally,
forests help to moderate climate and to maintain soils and precipitation patterns;
globally, forests also help to moderate weather patterns and stabilize water cycles (Sayer
and Whitmore, 1991). Although many of the local and global environmental services of
forests also can be provided by modified vegetation cover, loss of species' habitat and
biodiversity cannot.
2.8.1.2. Hypotheses
The main cause of deforestation is direct human clearing, although the reasons
differ somewhat for tropical versus temperate forests.
14There is some controversy over the exact estimates owing to varying definitions of 'deforestation'
(Sayer and Whitmore, 1991).
15 According to the New York Times, the National Space Research Institute reported that Landsat
satellite images revealed that 27 percent less forest was lost in Brazil in 1990 than in 1989 (NYT, 1991).
121
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Exhibit 2.8.1. Percent of original forest cover remaining in the United States and
Middle America since 1500.
100 -,
CD
O
O
§
80 -
60 -
O
LL.
75
c
B>
2 40
o
o
O)
CO
20 -
United States
Middle America
1500 1600 1700 1800
Year
1900
—r
2000
In the Untied States, the early deforestation of the 1700's and 1800's has been reversed in
recent years, with reforestation of previously agricultural lands in the eastern states. The
reverse is true in Middle America (Le., Mexico, Central America, and the Caribbean Islands),
where the recent deforestation trends continue. A picture similar to that for Middle America
might result for South America.
Source: Powell and Rappole, 1986.
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Tropical rainforests. Tropical closed forests are cleared primarily for three reasons:
(1) for agriculture to feed growing populations, (2) for cash crops .such as beef cattle to
earn foreign exchange, and (3) logging of hardwoods (WRI, 1990). Agricultural
conversions can reflect a government policy to expand the agricultural base (e.g., as in
Indonesia) or to resettle people (e.g., as in Brazil's state of Rondonia). Agricultural
conversion also occurs as a result of lack of policy or conflicting policies (WRI, 1990).
Governments also have provided economic incentives for deforestation for cash crops
(e.g., Brazil), despite the fact that some practices (e.g., cattle ranching) are not
sustainable on the poor tropical soils. Even selective logging can result in several forest
degradation. Although only some species of trees, accounting for 10 to 20 percent of the
forest, are of commercial value, the techniques used to log these trees can result in
destruction of another 30 to 50 percent of the forest trees (WRI, 1990). Also, the soils
can be so compacted and disturbed as to impede forest regeneration (WRI, 1990).
Another cause of deforestation is demand for fuelwood and fodder where the local
resources cannot meet demands (WRI, 1990).
US Pacific Northwest. The coastal region of Oregon, Washington, and northern
California, reaching inland to the western slopes of the Cascade Mountains, used to be
covered with conifer forests characterized by very old (i.e., more than 250 years), large
trees such as Douglas fir and Ponderosa pine. Nearly all of the old growth on private
lands in the Pacific Northwest has already been logged (Morrison, 1988). The remaining
old growth is located in 12 national forests administered by the US Forest Service (WS,
1988). In 1950, 3.5 billion board feet of timber were harvested in national forests; by
1990, the harvest had increased to 10.5 billion board feet (Lemonick, 1991*P). With
respect to old growth alone, 170 acres were being cut daily by 1987 (WS, 1988).
US Northeast. There are 32 million acres of forest in New York and northern
New England, where private ownership is the norm (95 percent of the forests in Maine
are privately owned, 98 percent in New Hampshire, and 85 percent in Vermont). Paper
companies, which own a large proportion of the forests, are finding that the value of the
land for real-estate development now far exceeds the value of the land for logging (Gold,
1989*P; Daly, 1989*P). Already large tracts have been sold to developers, and without
economic disincentives, this pattern is likely to continue (Daly, 1989*P).
2.8.2. Declines and Diebacks
2.8.2.1. Description
Background. Declines and "diebacks" in north temperate forests began first in
Europe and then developed in the United States and Canada in the 1970's (Klein and
Perkins, 1987; Siccama et al., 1982; Scott et al., 1984; McLaughlin et al., 1986). In
Europe, forest decline was initially noticed only in stands of silver fir (Abies alba), Tout
later spread to include other coniferous species (Norway spruce) and hardwoods such as
oak, maple, and ash (Cowling, 1989; Mueller-Dombois, 1988). The most common
123
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symptoms include chlorosis and visible
thinning of tree crowns, decrease in
growth and root biomass, and changes
in the shape and size of leaves (Schutt
and Cowling, 1985; Cowling, 1989).
The declines of many different forest
ecosystems that have taken place
recently have been called neuartige
Waldschaden (i.e., new type of forest
damage; Kandler, 1990; Tomlison et
al., 1990) and Waldsterben (i.e., forest
death) has been used to describe the
consequences of the damage (Blank,
1985; Schutt and Cowling, 1985;
Tomlison et al., 1990). The new forest
decline is found mostly in elevated areas (Krause, 1989).
Trends. In West Germany, the percentage of Norway spruce exhibiting symptoms
of decline increased from 8 to 52 percent of all West German trees between 1982 and
1987 (Raloff, 1989a). The situation for forests in eastern block countries may be
substantially worse (Mazurski, 1990). As of 1987, overall 15 to 20 percent of the
coniferous trees and 30 to 40 percent of the deciduous trees were affected in European
countries (Krause, 1989).
In the United States, an area in which forest decline and dieback is most apparent
is the Appalachian Mountains from Vermont to North Carolina, in particular in New
York, New Hampshire, and Vermont (Cowling, 1989). Decreases in radial growth have
been detected in low elevation red spruce in New York and several New England states
(Hornbeck and Smith, 1985; as cited in Cowling, 1989) and in natural stands of loblolly,
slash, and shortleaf pines in North and South Carolina, Georgia, Alabama, and Florida
(Sheffield et al., 1985; as cited in Cowling 1989).
Forest decline also may be occurring in Pacific countries (Old et al., 1981;
Warwick and Watt, 1983; Mueller-Dombois and McQueen, 1983; summarized by Mueller
Dombois, 1988).
2.8.2.2. Hypotheses
Although there is a possibility that forest diebacks are part of a natural cycle, "the
current problem is unique in that serious dieback and loss of tree vigor have occurred,
with both conifers and hardwoods in different types of ecosystems, in several industrial
countries in less than one decade" (Tomlinson, et al., 1990). The majority of the
scientific community believes that recent forest diebacks in industrialized countries are in
response to air pollution and a combination of direct and indirect effects of that pollution
124
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(Exhibit 2.8.2) (Bucher and Bucher-Wallin, 1989; Grossman, 1988; Heliotis et al., 1988;
Hinrichsen, 1986; Kander, 1990; Schulze, 1989; Schutt and Cowling, 1985; Tomlison et
al., 1990; Tovar, 1989). Three direct stresses are associated with air pollution, i.e.,
elevated levels of ambient ozone and sulfur dioxide, acid deposition (from the
combustion of fossil fuels), and nitrogen deposition (from agricultural sources). Indirect
stresses include the effect of acid deposition on soil chemistry (e.g., leaching of nutrients
and elevated levels of aluminum ions). Both direct and indirect stresses may have effects
on tree root and foliage vigor and function. Weakened trees can become more
susceptible to other natural stresses such as drought, insect pests, and temperature
extremes. Global warming and biological nutrient mining also may contribute to forest
dieback. We discuss each of these briefly below. .
Air Pollution , ,
Gaseous pollutant injury -- ozone and sulfur dioxide. Unlike other gaseous
pollutants, concentrations of ozone in areas remote from urban and industrial sources
tend to be higher at greater altitudes, a pattern which corresponds with the observed
greater forest damage at higher altitudes (Frank, 1991; Krause, 1989). The adverse
effects of ozone in coniferous forests have been well documented (US EPA, 1986; US
EPA, 1987; Norse, 1990). Effects of ozone on herbaceous and woody vegetation include
foliar injury, reduction in growth and yield, and increased susceptibility to pests and
pathogens (US EPA, 1987). Ozone has been known to damage vegetation in
concentrations as low as 0.1 to 0.2 ppm for periods of six hours over several days
(Hinrichsen, 1986). Two large-scale studies in the United States conclusively linked
ozone pollution to forest damage, one in the San Bernardino Mountains east of Los
Angeles, California, and the other in Virginia (Bartuska et al., 1985, as cited by
Hinrichsen, 1986). Ozone has been demonstrated to be responsible for visible injury and
decreased growth in some individual eastern white pine trees (Berry and Hepting, 1963;
Hayes and Skelly, 1977; Benoit et al., 1982) and in southern California forests (Parmeter
et al., 1962; Ohmart and Williams, 1979). Tomlison et al. (1990) have concluded,
however, that the hypothesis that elevated ozone levels are the primary cause of forest
damage in Germany (Prinz et al., 1982; Prinz, 1983) is not supported by available data.
In addition to ozone effects, European forest Waldsterben has been attributed in
some areas to direct effects of SO2 (Ulrich, 1990). Sulfur dioxide injures trees by
entering the leaves (or needles) through their stomata (pores), where it reacts with water
to produce sulfuric acid. Deciduous leaves take on a "bleached" look, whereas conifer
needles turn red-brown (Hinrichsen, 1986). Gradients of SO2 concentration and
vegetation damage with distance from an SO2 source have made it relatively easy to
study the effects of SO2 on vegetation (Krause, 1989). Crop, forest, and vegetation
damage have occurred in the vicinity of fossil fuel power plants and metal smelters which
emit high levels of SO2 (Hinrichsen, 1986). Although elevated SO2 levels have been
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Exhibit 2.8.2. Comparison of symptoms and possible causes of forest declines
in central Europe and eastern North America.
Possible Causative Agent Symptoms
Foliar Leaching, Ozone,
Drought
Natural Stress, Abiotic and
Biotic
Insect Pests, Drought
Fertilization
Chronic Ozone, Chronic
SO2
Acute Ozone, Acute SO2
Foliar Fertilization
Ozone
Stress
Stress, N Fertilization
Yellowing of foliage from
the lower to the upper and
from the inner to the outer
portion of branches—oldest
tissues affected first.
Dying back from the top
of trees—youngest tissues
affected first.
Increased transparency of
crowns due to gradual loss
of leaves but with leaves
retained to the very top of
the trees.
Losses of fine-root biomass
and mycorrhizae
. (beneficial symbiosis
between tree roots and soil
fungi).
Synchronized decrease in
diameter growth without
other visible symptoms.
Synchronized decrease in
diameter growth with other
visible symptoms. May
result in mortality.
Concentration of leaves
and needles at tips of
branches in tufts or
clumps.
Excessive production of
adventitious shoots on
branches.
Excessive production of
seeds and cones.
Central Europe
Observed mainly in white
fir and Norway spruce at
high elevation.
Common in oak and ash,
less common in birch and
beech.
Observed in Norway
spruce, white fir, Scots
pine, larch, beech, birch,
oak, maple, ash, and alder.
Common in white fir,
Norway spruce, and beech.
Not studied in other
species.
Not reported in Europe.
Studied mainly in Norway
spruce, white fir, and
beech. Not studied in
other species.
Common in oak and ash.
Common in Norway
spruce, white fir, and larch.
Common in spruce, fir,
beech, and birch; often
observed several years in a
row.
Eastern North America
Observed with white fir in
the San Bernardino
Mountains and recently in
red spruce in New York
and Vermont.
Conspicuous in red spruce;
maple and oak declines;
ash and birch diebacks.
Observed only in the
littleleaf disease of
shortleaf pine and in the
beech-bark disease.
Observed mainly in red
spruce decline, birch
dieback, and littleleaf
disease.
Observed in pitch pine and
shortleaf pine.
Observed in red spruce
and Fraser fir mainly at
high elevation.
Observed in nearly all
decline of broad-leaved
trees and in some conifers.
Observed recently for the
first time in conifers.
Common in maple and
oak, ash, and birch.
Observed in many stressed
trees mainly one year at a
time.
Source: Adapted from Hinrichsen, 1986.
126
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found in several areas in Europe that are experiencing severe forest declines, SO2 levels
are not elevated in other areas experiencing declines (Krause, 1989). .
Acid deposition. Both wet and dry (sorbed to particulates) acid deposition occurs
in north temperate forests. Wet deposition occurs through rain, snow, dew, and fog; the
pH of rain water in industrialized areas typically is around 4.2 (Krause, 1989). The direct
and indirect contributions of acid deposition to forest diebacks remain controversial,
however. Direct effects of acid deposition may be reduced growth, premature defoliation
in the autumn, and changes in sap chemistry, but long-term studies still are needed (Erb,
1987*P). Indirect effects of acid deposition include root damage from aluminum toxicity,
aluminum blocking of nutrient uptake, leaching of essential nutrients from the soil, and
leaching of nutrients from foliage.
Increased acidity of soils increases the mobility of metal cations such as aluminum,
which can be directly toxic to roots at high concentrations (Godbold et al., 1988; Shortle
and Smith, 1988) and which can competitively block root uptake of other positively
charged ions that are essential nutrients (e.g., magnesium, calcium; studies summarized
by Tomlison et al., 1990). Furthermore, increased soil acidity helps to leach essential
nutrients such as calcium and magnesium from the soil and to create an ionic imbalance
in the soil that has deleterious effects on trees' fine roots (Ulrich, 1983). The resulting
moisture and nutrient stress weaken the trees, which can then succumb to pathogens,
weather, and other stressors that they might have withstood in the absence of acid rain
(Ulrich, 1990; Tomlison et al., 1990).
Rehfuess (1981) proposed that acid deposition also may increase the rate of
leaching of calcium, potassium, and magnesium directly from foliage. A program in
Munich, Germany, designed to test this hypothesis found that magnesium and/or calcium
deficiency in trees exposed to ozone and acid fog results primarily from inadequate
uptake of these nutrients from the soil, with the result that nutrient leaching from foliage
only becomes a problem when there is an insufficient supply in the soil (Tomlison et al.,
1990). Some degree of foliar leaching is considered a normal part of trees' nutrient
cycling, and there appears to be no conclusive evidence that this factor is a primary cause
of forest decline (Hinrichsen, 1986).
Excess nitrogen deposition. North American studies have found that 10 percent of
all agriculturally applied quantities of nitrogen fertilizers evaporate into the atmosphere
(Hinrichsen, 1986). In the higher elevation spruce-fir forests of the northeastern United
States, atmospheric deposition of nitrogen has been estimated to be as high as 37 to 44
kg/hectare-year, with half of it coming down as wet deposition (Bartuska et al., 1985).
Nitrogen oxides deposited on foliage as well as in the soil can be absorbed by trees.
Nitrogen deposition on soils can stimulate nitrification and nitrate leaching, which
increases soil acidity and can contribute to the stresses described in the previous
paragraph (Johnson and Taylor, 1989). Excess nitrogen uptake can stimulate trees into
extra growth activity, preventing them from preparing for winter (i.e., sequestering
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carbohydrates and other substances during the "hardening" process; Hinrichsen, 1986).
Although some believe that growth stimulated by atmospheric nitrogen uptake has
caused magnesium deficiencies in some European forests (Schulze, 1989), the evidence is
as yet circumstantial. Evidence linking excess nitrogen oxides to forest decline in the
United States also is circumstantial.
Other gaseous pollutants. A further possibility receiving attention recently is that
airborne halocarbons, particularly 1,1,1-trichloroethane and tetrachloroethene, are
photooxidized at the higher altitudes to the herbicide trichloroacetic acid (TCA), but
additional research is needed to evaluate this possibility (Frank, 1991).
Other Stressors
Natural fluctuations. Some researchers have proposed that forest diebacks are
part of natural cyclic fluctuations. Skelly (1989) suggests that pollutant deposition and
naturally occurring forest stressors (e.g., pathogens, drought) occur over the same regions
and elevational gradients, which make natural and anthropogenic stressors difficult to
distinguish. Kandler (1990) compared old photographs of trees in several forests in West
Germany with pictures of the same trees today and reviewed reports on tree condition in
the early 1920s. He concluded that the Waldstefben complex may be part of a natural
fluctuation, or at least not a new phenomenon since the turn of the century. Weather
extremes, particularly drought (Krause, 1989), may have contributed to some instances of
forest dieback over the past century (Tomlison et al., 1990). Long-lasting dry periods
may significantly increase forests susceptibility to many kinds of disease and pest
outbreaks (Krause, 1989).
Pathogens. Although some localized areas of dieback have been attributed to
outbreaks of specific pathogens (e.g., fungi, insect pests), these outbreaks may occur
more frequently in trees already weakened by anthropogenic pollution. In the studied
examples of forest declines and diebacks, pathogens have usually been described as
"accelerating" causes, and sometimes "triggering" causes, but almost never as
"predisposing" causes (AIBS, 1987; Franklin et al., 1987; Manion, 1981; Houston, 1981;
Warwick and Watt, 1983; as cited in Mueller-Dombois, 1988).
An important problem, however, is the loss of specific tree species to introduced
pathogens. In North America, the chestnut and elm have been all but wiped out in
North America by imported diseases (i.e., chestnut blight and dutch elm disease). Now,
the eastern hemlock appears to be threatened with extinction in the wild by an insect
apparently imported from Japan (Stevens, 1991*P). In Oregon and Washington states,
past logging and fire prevention practices have resulted in the ponderosa pines being
replaced by dense stands of firs and lodgepole pine. These species are more vulnerable
to insect pests and large tracts have died from repeated insect pest outbreaks
(Kenworthy, 1992*P).
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Biological nutrient mining. Monoculturing of a single tree species (e.g., Norway
spruce), cutting stands before they became senescent, and preventing natural
regeneration of soil nutrients also may have contributed to the observed soil-nutrient
deficiencies in Europe, particularly in spruce forests (Mueller-Dombois, 1988). Although
evidence is lacking, negative consequences of repeated spruce monocultures are
beginning to receive serious attention (Bourdeau, 1987). Whether the observed soil
nutrient deficiencies are a result of leaching of nutrients due to soil acidification or of
biological nutrient mining, experimental fertilization of German forests with the needed
nutrients has succeeded in restoring tree vigor, and parts of Germany are developing
plans for large-scale forest fertilization and rehabilitation (Tomlison et al,, 1990).
Global warming. The scientific community has not reached a consensus on the
possible contribution of global warming to north temperate forest dieback; however, it is
an area of intense research. Unusual extremes in temperature or rainfall may kill trees
already weakened by atmospheric pollution. .
2.8.3 Continued Monitoring
Deforestation .
The United Nations Food and Agriculture Organization (FAO) and the United
Nations Environment Program (UNEP) sponsored the 1980 and 1990 Tropical Forest
Resources Assessments. The 1990 assessment was based on remote sensing data from
the National Oceanic and Atmospheric Administration and Landsat satellites. Various
researchers and organizations with access to the Landsat data will continue to follow
deforestation trends with these data.
Forest dieback
The Forest Ecosystems and Atmospheric Pollution Research Act of 1988 directed
the United States Department of Agriculture (USDA) Forest Service (FS) to establish a
monitoring system to track long-term trends in the health and productivity of forests and
related ecosystems in the United States. The FS maintains a forest timber inventory data
base and recently has been designing a Forest Health Monitoring (FHM) system in
response to concerns about the potential effects of global climatic change on forests
worldwide (CEQ, 1990). The FHM was implemented in the six-state New England
region in 1990 with cooperative efforts of the FS and EPA. Forest conditions will be
described using five 'health' indicator groups: growth, foliage symptomatology, soil
chemistry, foliar chemistry, and landscape characterization (Brooks et al., 1991). Other
investigators are contributing to the effort as well. For example, Tritton and Siccama
(1990) recently reviewed 46 primary data sets to estimate the proportion of standing
trees in the northeastern United States that are dead to serve as a baseline for future
studies.
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The Federal Republic of Germany established their Forest Damage Inventory in
1983 and has conducted annual surveys of their forests since. The only damage
symptoms considered, however, are leaf loss and leaf discoloration. The European
Forest Ecosystem Research Network (FERN) has been coordinating surveys of forests in
several European countries for the past five years. Other European and Canadian
vegetation condition surveys also have been conducted by various agencies and
institutions over the last 20 years.
2.8.4. References
Bartuska, A, et al. 1985. Assessment of acid deposition and its effects. Washington,
DC: NAPAP, draft contribution, 1985.
Benoit, LF, Skelly, JM, and Moore, ID, et al. 1982. Radial growth reductions of Pinus
strobus L. correlated with foliar ozone sensitivity as an indicator of ozone induced losses
in eastern forests. Can. J. For. Res. 12:673-678.
Berry, CR, and Hepting, GH. 1963. Ozone, a possible cause of white pine emergence
tipburn. Phytopathology 53:552-557.
Blank, LW. 1985. A new type of forest decline in Germany. Nature (Lond.)
314:311-314.
Bourdeau, P. 1987. Trends Ecol. Evol. 2:236-237.
Brooks, RT, Miller-Weeks, M, and Burkman, W. 1991. Summary Report - Forest
Health Monitoring, New England, 1990. Northeastern Area Association of State
Foresters and USDA, Forest Service. Northeastern Area, Northeastern Forest
Experiment Station. Rep. No. NE-INF-94-91.
Bucher, JB, and Bucher-Wallin, I (eds.). 1989. Air Pollution and Forest Decline Vols. I
and II, 14th International Meeting for Specialists in Air Pollution Effects on Forest
Ecosystems, Interlaken, Switzerland, October 2-8, 1988. Birmensdorf, Switzerland:
Eidgenoessische Anstalt Fuer Das Forstliche Versuchswesen.
CEQ. 1990. Environmental quality. Twentieth annual report. The Council on
Environmental Quality. The Executive Office of the President.
Cowling, EB. 1989. Recent changes in chemical climate and related effects on forest in
North America and Europe. Ambio 18:167-171.
Frank, H. 1991. Airborne chlorocarbons photooxidants and forest decline. Ambio
20:13-18.
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Franklin, JF, Shugart, GG, and Harmon, ME. 1987. BioSci. 37:550-556.
Godbold, DL, Fritz E., and Huettermann, A. 1988. Aluminum toxicity and forest
decline. Proc. Natl. Acad. Sci. USA 85:3888-3892,
Grossman, W-D. 1988. Products of photo-oxidation as a decisive factor of the new
forest decline results and considerations. Ecol. Model. 41:281-306,
Hayes, EM, and Skelly, JM. 1977. Transport of ozone from the Northeast U.S. into
Virginia and its effect on eastern white pines. Plant Dis. Rept. 61:778-782.
Heliotis, FD, Karandinos, MG, and Whiton, JC. 1988. Air pollution and the decline of
the fir forest in Parnis National Park near Athens Greece. Environ. Pollut. 54:29-40.
Hinrichsen, D. 1986. Multiple pollutants and forest decline. Ambio 15:258-265.
Hornbeck, JW, and Smith, RB. 1985. Documentation of red spruce growth decline.
Can. J. For. Res. 15:1199-1201. ,
Houghton, RA. 1990. The global effects of tropical deforestation. Environ. Sci.
Technol. 24:414-422. . ,
Houston, DR. 1981. Stress triggered diseases: The diebacks and declines. USDA
Forest Service. NE-INF-41-81.
Hunt, FA. 1989. A hoot for the future; the spotted owl may answer a loaded question:
Is sustainable management possible in Northwest forests? American Forests 95:30-36.
Johnson, DW, and Taylor, GE. 1989. Role of air pollution in forest decline in eastern
North America. Water Air Soil Poll. 48:21-44.
Kandler, O. 1990. Epidemiological evaluation of the development of Waldsterben in
Germany. Plant Dis. Rept. 74:4-12.
Klein, RM, and Perkins, TD. 1987. Cascades of causes and effects of forest decline.
Ambio 16:86-93.
Krause, GH. 1989. Forest decline in central Europe: The unravelling of multiple
causes. In: Grubb, PJ, and Whittaker, JB (eds.), Toward a More Exact Ecology; Second
Jubilee Symposium of the 75th Anniversary of the British Ecological Society, Oxford,
England, UK, September 13-15, 1988. Boston, MA: Blackwell Scientific Publications.
Manion, PD. 1981. Tree disease concepts. Englewood Cliffs, NJ: Prentice Hall.
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Mazurski, KR. 1990. Industrial pollution: The threat to Polish forests. Ambio 19.
McLaughlin, SB, Blasin, TJ, and Downing, DJ, et al. 1986. Regional responses of red
spruce to environmental stress. In: Proceedings of the Third Annual Acid Rain
Conference for the Southern Appalachians, Gatlinburg, TN, December 1986.
Chattanooga, TN: Tennessee Valley Authority. Pp. 16-17.
Morrison, PH. 1988. Old growth in the Pacific Northwest: A status report. Washington,
DC: The Wilderness Society.
Mueller-Dombois, D. 1988. Forest decline and dieback: A global ecological problem.
Trends Ecol. Evol. 3:310-312.
Mueller-Dombois, D, and McQueen, DR. 1983. Canopy dieback and dynamic processes
in Pacific forests. Pac. Sci. 37.
Myers, N. 1989. Deforestation rates in tropical countries and their climatic implications.
Friends of the Earth, London.
Norse, EA. 1990. Ancient forests of the Pacific Northwest. Washington, DC: Island Press.
Ohmart, CP, and Williams, CB, Jr. 1979. The effects of photochemical oxidants on
radial growth increment for five species of conifers in the san Bernardino National
Forest. Plant Dis. Rept. 63:1038-1042.
Old, KM, Kile, GA, and Ohmart, CP. 1981. Eucalypt dieback in forests and woodlands.
In: Proc. Conf. CSIRO Div. For. Res., Canferra, Australia.
Parmeter, JR, Jr., Gefa, RV, and Neff, T. 1962. A chlorotic decline of ponderosa pine
in southern California. Plant Dis. Rept. 46:269-273.
Powell, GV, and Rappole, JH. 1986. The hooded warbler. Audubon Wildl. Rep. 1986.
New York, NY: National Audubon Society. Pp. 827-853.
Prinz, B. 1983. Gedanken zum Stand der Diskussion uber die Urache der Waldschaden
in der Bundesrepublik Deutchland. Forst Holzwirt 38:460-468.
Prinz, B, Krause, GH, and Stratmann, H. 1982. Waldschaden in der Bundesrepublik
Deutschland, LIS Berichte 28. State Institue for Pollution Control of the State of North
Rhine Westphalia, Essen, FRG.
Raloff, J. 1989a. Where acids reign: Do dying stands of Bavarian timber portend the
future of polluted US forests? Science News 136:56-58.
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Rehfuess, KE. 1981. Uber die Wirkungen des sauren Niederschlage in
Waldokosystemen. Forstwiss. Centralbl. 100:363-381.
Sayer, JA, and Whitmore, TC, 1991. Tropical moist forests destruction and species
extinction. Biol. Conserv. 55:199-213. . . .
Schulze, ED. 1989. Air pollution and forest decline in a spruce (Picea abies) forest.
Science 244:776-783. ,
Schutt, P, and Cowling, EB. 1985. Waldsterben, a general decline of forests in central
Europe: Symptoms, development, and possible causes. Plant Dis. Rept. 69:548-558.
Scott, JT, Siccama, TG, and Johnson, AH, et al. 1984. Decline of red spruce in the
Adirondacks, New York. Bull. Torrey Bot. Club 111:438-444.
Sheffield, RM, Cost, ND, and Bechtold, WA, et al. 1985. Pine growth reductions in the
southeast. Ashville, NC: USDA Forest Service, Southeast Forestry Experimental
Station. Resour. Bull. SE-83.
Shortle, WC, and Smith, KT. 1988. Aluminum-induced calcium deficiency syndrome in
declining red spruce. Science 240:1017-1018.
Siccama, TG, Bliss, M, Vogelmann, HW. 1982. Decline of red spruce in the Green
Mountains of Vermont. Bull. Torrey Bot. Club 109:162-168.
Skelly, JM. 1989. Forest decline versus tree decline -.the pathological considerations.
Environ. Monitor. Assess. 12:23-27.
Tomlinson, GH, et al. (eds.). 1990. Effects of acid deposition on the forests of Europe and
North America, Boca Raton, FL: CRC Press. 213 pp.
Tovar, DC. 1989. Air pollution and forest decline near Mexico City, Mexico. Environ.
Monitor. Assess. 12:49-58.
Tritton, LM, and Siccama, TG. 1990. What proportion of standing trees in forests of the
northeast USA are dead? Bull. Torrey Bot. Club 117:163-166.
Ulrich, B. 1983. An ecosystem oriented hypothesis on the effect of air pollution on
forest ecosystems. In: Ecological effects of acid deposition. Solna, Sweden: National
Swedish Environment Protection Board. Report PM 1636.
Ulrich, B. 1990. Waldsterben forest decline in West Germany. Environ. Sci. Technol.
24:436-441.
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US EPA. 1986. Review of the national ambient air quality standards for ozone,
preliminary assessment of scientific and technical information. Research Triangle Park,
NC: US Environmental Protection Agency, Office of Air Quality Planning and
Standards. .
US EPA. 1987. Appendix III. In: Unfinished business: A comparative assessment of
environmental problems. Washington, DC: US Environmental Protection Agency,
Office of Policy, Planning and Evaluation, Ecological Risk Workgroup.
Warwick, BS, and Watt, V. (eds.). 1983. The future of Tongariro National Park beech
forests. Wellington, New Zealand: Dept. Lands and Survey.
WRI. 1988. Forests and Rangelands. In: World Resources 1988-89. World Resources
Institute and the International Institute for Environment and Development (WRI/IIED).
New York, NY: Basic Books, Inc.
WRI. 1990. Forests and Rangelands. In: World Resources 1990-91. World Resources
Institute and the International Institute for Environment and Development (WRI/IIED).
New York, NY: Basic Books, Inc.
WS. 1988. End of the ancient forests - Special report on National Forest plans in the
Pacific Northwest, Washington, DC: The Wilderness Society.
2.8.5. Popular Press Bibliography
AP (Associated Press). 1990. Rate of tropical forest loss to exceed earlier estimates.
Washington Post. June 8, 1990.
Austin, P. 1991. Forests at risk: Shifting the fight to the Maine woods, (environmental
conservation efforts should focus on Northern Woods in New England and move away
from the Pacific Northwest). Los Angeles Times. July 7, 1991, p M2.
Booth, W. 1989. Tropical forest loss may be killing off songbirds, study says.
Washington Post. July 26, 1989, vol 112, col 3, pp Al, A28.
Brooke, J. 1991. Amazon forest loss is sharply cut in Brazil. New York Times. March
26, 1991, p B8.
Buckro, C. 1990. Environmentalists side with loggers: Threat of raiders brings foes
together. Washington Post. May/June, 1990.
Daly, CB. 1989. Development threatens Northeast timber; Forest Service study urges
revisions in tax policy as strategy to promote preservation. Washington Post. October
22, 1989, vol 112, col 1, p A3.
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Erb, C. 1987. The jury is still out. Pennsylvania State Agriculture (fall):2-ll.
Feeney, A. 1989. The Pacific Northwest's ancient forests: Ecosystems under siege!
Washington, DC: Audubon Wildlife Report, Academic Press.
Gold, AR. 1989. Developers' money threatening northern forests. New York Times.
April 10, 1989, vol 138, col 3,pp A7, A10.
JEN. 1988. Log imports said threatening tropical forest conservation. Japan Economic
Newswire. November 17, 1988.
Kenworthy, T. 1992. 'Unraveling' of ecosystem looms in Oregon forests; scientists say
recovery could take century. Washington Post, May 15, 1992, pp Al, A14.
Lemonick, MD. 1991. Whose woods are these? Time Magazine. December 9, 1991, pp
70-75.
Luoma, JR. 1989. Logging of old trees in Alaska is found to threaten eagles; US study
predicts long-term decline in Tongass forest. New York Times. November 7, 1989, vol
139, col 1, pp B7, C4.
Mathews, J. 1990. Scientists urge partial logging ban to save spotted owl. Washington
Post. April 6, 1990, p A16.
McLean, HE. 1990. Forest of torches: Millions of drought-weakened, beetle-killed
conifers are browning the Sierras and fueling fears of catastrophic fires. American
Forests 96:50-56.
O'Toole, R. 1990. The forest service's catch 22; it's hard to see the forest when you've
cut down all the trees. Washington Monthly 21:18.
Page, J. 1988. Clear-cutting the tropical rain forest in a bold attempt to salvage it.
Smithsonian 19:106.
Prochnau, W, and Hollister, A. 1990. Last stand for the old woods; much of what's left
of our primeval forests is about to vanish in a rampage of greed. The time has come to
just say no. Life 13:52(6).
Raloff, J. 1989b. Climate change: Boon to western trees? Science News 136:127.
Reidel, C. 1990. The northern forest: Our last best chance (Whose woods are these?).
American Forests 96:22-28.
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Rowen, H. 1989. Heading off an Amazon disaster. Washington Post. April 2, 1989, vol
112, col 3, p HI.
Shabecoff, P. 1990. Loss of tropical forests is found much worse than was thought. New
York Times. June 8, 1990, pp Bl, B6.
Shapiro, H. 1988. Destruction of rain forests, warns a conservationist, is endangering
many species - including our own. People Weekly 30:165.
Simon, JL. May 1986. Disappearing species, deforestation, and data. New Scientist
60-63.
Skow, J. 1988. In Washington: Lighthawk counts the clear-cuts. Time 132:12.
Stevens, WK. 1991. Time is running out for eastern hemlock; a destructive insect
approaches the tree's heartland. New York Times. November 26, 1991, p C4.
Warshall, P. 1989. The political economy of deforestation. Whole Earth Review
(fall):68.
Watson, J. 1990. The last stand for old growth. National Wildlife 28:24-25.
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3. CONCLUSIONS
In our literature review, we identified several biological populations as potential
indicators of large-scale environmental change. In this report, we summarized
hypotheses and supporting evidence for the observed trends for eight potential indicators
of environmental change which have received the most attention in the recent popular
press (with the exception of loss of wetlands and loss of biodiversity for which EPA has
initiated other focused research efforts). The eight indicators covered in this volume are
groups of animals or plants for which populations are or appear to be declining and in
some cases, going extinct, more rapidly in the past few decades than in previous years.
While there are examples of species that are increasing in abundance and expanding
their ranges (e.g., cowbirds, fire ants, killer bees), the majority of these species represent
introduced generalist species that have successfully colonized an area in which they did
not evolve, and therefore have no natural controls. The expansion of populations of
introduced species is often detrimental to a diversity'of more specialized native species,
as is the case for North American fish, neotropical migrant birds, and probably
amphibians.
Available evidence indicates that human activities are contributing to many of the
observed population declines described in this report. The direct destruction,
degradation, and fragmentation of habitats as lands and waters are converted and altered
for human use appear to be the major contributors to declines in populations of
neotropical songbirds, ducks, freshwater fish, and turtles in North America. It is not yet
clear whether the apparent decline in amphibian populations worldwide is real, and if so,
what the cause(s) of the trend might be. Increasing environmental pollution is taking its
toll on the surface water quality upon which our fish fauna depend, and may have
contributed to the recent deaths and declines of dolphins and seals in the North Atlantic
and Mediterranean. In addition to suffering from physical destruction, nutrient runoff,
sedimentation, and other pollution, coral reef communities may be suffering directly from
a global ocean warming trend or increased variability in ocean temperatures. The
clearing of tropical rainforests not only threatens global biodiversity, but also the services
supplied by those forests in stabilizing our global climate.
In Section 3.1, we review the eight potential indicators to identify the relative
sensitivity of each of the groups of organisms to different anthropogenic stresses. We
then summarize those human activities that are causing or are likely to be causing the
observed declines in the eight groups (Section 3.2). Finally, in Section 3, we discuss some
of the difficulties associated with trying to use any of these groups of organisms as
indicators of large-scale environmental change.
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3.1 Summary of Relative Sensitivity of Biological Indicators
In this section, we review some of the life-history attributes of the eight groups of
organisms that help to determine their relative sensitivity to different categories of
anthropogenic stress. As described below, each group is sensitive to a different suite of
environmental stressors, and therefore may provide different windows by which to view
environmental change and quality.
Neotropical migrant birds. Neotropical migrant birds share several life-history traits
that make them particularly vulnerable to fragmentation of north temperate forests.
They tend to build open nests near to the ground and to lay only a single small clutch of
eggs each year. These traits have made neotropical migrant bird species vulnerable to
forest edge predators and parasites. With increasing ratios of forest edge to forest
interior, edge predators and parasites have access to an increasing proportion of the
neotropical migrant species, which are adapted to forest interior, not forest edge,
conditions. Neotropical migrant birds also are sensitive to changes in the tropical forests
in which they overwinter.
North American freshwater fish. The continued existence of native North American
freshwater fish species depends not only upon the chemical integrity of our surface
waters, but also upon the variety of physical conditions inherent in natural springs, rivers,
lakes, and estuaries which is lost when rivers are channelized and impounded. Formerly,
the southwestern United States supported a high diversity of native fish species because
of the numerous, yet isolated, drainage systems and surface water bodies. The relatively
small and isolated populations of native fish species in these areas are particularly
vulnerable to habitat destruction and the diversion of water for human agricultural,
industrial, and domestic uses.
Ducks. Duck populations depend on wetland habitats for breeding, for stopovers
during migration, and for overwintering. Thus, ducks are sensitive to drought and human
activities that reduce the availability of wetland habitats. Waterfowl are also particularly
susceptible to chemical pollution of their aquatic feeding habitats.
Coral reefs. Limited in distribution to waters warm enough for coral organisms to
precipitate calcium carbonate from seawater and clear enough to permit sunlight to reach
the microscopic plants that live symbiotically in their tissues, corals are vulnerable to any
human activities that degrade this environment. Living in areas that represent the
warmer extremes of the evolution of aquatic life on the planet, scientists are concerned
that corals may be unable to adapt to ocean warming trends. Coral reef communities
also require many years to recover from major destruction.
Amphibians. The life-cycle and physiology of amphibians may render them more
susceptible to chemical pollution, extremes in weather, and acid deposition, than most
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other groups of organisms. The eggs of many amphibian species are laid in water and
have little physical protection from water-borne contaminants or unusual water
temperatures. Adult amphibians are carnivorous and therefore more vulnerable to
bioaccumulating environmental contaminants from their food than are animals lower in
the food chain (e.g., herbivores). In addition, the skin of most, amphibian species is
highly permeable, making them particularly susceptible to pollutants from air, water, or
other environmental media. Amphibians require moist habitats to prevent excessive
water loss through their highly permeable skins; they are therefore susceptible to
desiccation under unusually dry or hot weather conditions. Amphibian populations are
also very susceptible to physical destruction of aquatic habitats which are required for egg
and larval development in many species.
Turtles. Land turtles are vulnerable to fragmentation of their habitat by roads and
highways because of their relatively slow locomotion and large home ranges. Sea turtles
are particularly vulnerable to several categories of anthropogenic stress, including shrimp
trawling-induced mortality, pollution of the marine environment with toxic substances and
physical debris, direct exploitation, and several effects incidental to human presence and
developments on coastal beaches where sea turtles lay their eggs in the sand.
Dolphins and seals. Dolphins and other marine mammals are likely to be sensitive
to environmental pollution because of their position high in the marine food chain and
because of their relatively high body fat content, which helps minimize loss of body heat
in their cold marine environments. As top carnivores, dolphins and seals feed on fish
that may have accumulated toxic substances in their tissues both directly from the water
and from their food. Because of their large -fat reserves, dolphins and seals also can
store large quantities of toxic substances that accumulate in fatty tissues (e.g., PCBs).
Marine mammals are long-lived and can accumulate toxic substances from their
environment over many years.
Forests. Forests provide many invaluable services: they are responsible for
providing three-dimensional terrestrial habitat for a large diversity of animal species,
particularly in the tropics, for moderating temperatures, for maintaining precipitation
cycles, and for absorbing carbon dioxide, a greenhouse gas that can contribute to global
warming. Loss of forests results in loss of these ecosystem services, which can have
serious impacts many groups of organisms and the existence of many ecosystem types.
Moreover, loss of forest services in one area can adversely affect forests in adjacent areas
as precipitation and temperature patterns change. The health of forests depend on the
physical and chemical condition of the atmosphere and of the soils on which they grow.
Human activities that alter soil conditions (e.g., nutrient availability, moisture content), in
particular, can have devastating effects.
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3.2 Summary of Human Activities Causing Species Declines
As human populations and settlement areas continue to increase in the United
States and worldwide, human activities impinge on ever increasing areas of North
America and the planet. Exhibit 3 summarizes the human activities that the literature
review identified as being responsible or likely to be responsible for declines in the eight
groups of organisms evaluated in this review. In Exhibit 3, we group anthropogenic
stresses into three multiple stress categories (i.e., habitat alteration, toxic chemicals and
solid wastes, and combustion of fossil fuels) and two single stress categories (i.e.,
increasing introductions of non-native species and exploitation of resources, both direct
and incidental). We discuss each of these stress categories below.
Habitat alteration. The ever-increasing human population continues to directly
alter terrestrial and aquatic ecosystems for purposes of agriculture, industry, suburban,
and urban developments. Filling of wetlands, clear-cutting or burning forests, building
roadways and power transmission lines that fragment the remaining forests, and other
activities associated with converting lands for human uses are major contributors to the
loss and degradation of terrestrial habitats. These activities result in the loss of wetland
and forest ecosystems and fragmentation of the remaining habitats. These activities also
further isolate the remaining habitat islands increasing the probability of local population
extinctions as a consequence of natural variation in mortality and reproductive success.
These activities also can dramatically alter the condition of the remaining habitat. For
example, deforestation, particularly in riparian areas (i.e., along rivers), causes increased
surface water temperatures (less shade) and increased sedimentation (from runoff). For
aquatic habitats, direct modification of surface water bodies (e.g., stream channelization,
construction of dams, impoundments, and reservoirs) reduces physical habitat diversity
and water flow, causing loss of fish species and possibly amphibians that had filled a
variety of specialized niches and habitat types. Direct habitat alteration is considered to
be responsible for the majority of the extinctions and reductions in populations of North
American freshwater fish, neotropical migrant birds, and possibly amphibians, and is
considered to contribute strongly to the declines of ducks and both land and sea turtles.
Runoff of fertilizers and other nutrients (e.g., manure) from agricultural areas has
resulted in eutrophication of inland surface waters and degradation of coral reef
communities which evolved in low nutrient areas of the ocean. Increasing sedimentation
from runoff from urban and suburban developments, logging and mining operations, and
agriculture also have degraded both inland freshwater and coastal marine ecosystems.
Tropical rain forests are among the most species-rich habitats on earth.
Deforestation in the tropics is seriously reducing global biological diversity. In North
America, we may already be seeing consequences of tropical deforestation in the diversity
of our own bird communities, as the abundance and distribution of neotropical migrant
birds declines. We soon may feel other effects as we lose the precipitation and climate
moderation services provided by these forests as well as their ability to serve as a sink for
carbon dioxide, a gas that can contribute to global warming.
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Production of toxic chemicals and solid wastes. The second group of multiple
anthropogenic stressors listed in Exhibit 3 result from increasing and changing releases of
man-made toxic substances and solid wastes into the environment as human populations
expand, despite efforts to curtail releases. Sewage contributes to the degradation of
aquatic ecosystems by increased sedimentation and biological oxygen demand (BOD) as
well as by increasing concentrations of toxic substances in some surface waters.
Emissions to the atmosphere from motor vehicles, industrial sources, and agriculture
include substances that are directly toxic to vegetation and that can adversely modify soil
chemistry. Air pollution is believed to be a primary cause of forest dieback in
industrialized countries. Other chemical pollutants of concern include those that
bioaccumulate in terrestrial and aquatic food chains to levels that have adverse effects on
animals at the top of the food chain (e.g., bald eagles and osprey prior to bans on PCBs
and DDT; now possibly dolphins and other marine mammals potentially due to these
chemicals accumulating in the ocean). Pesticides from agricultural fields is another
source of continuing environmental pollution that may be causing adverse effects on
aquatic invertebrates and the ducks that feed on them. A more recent problem is
increasing levels of physical debris in the environment, particularly plastics in the ocean
which are ingested by or entangle sea turtles and marine mammals.
Fossil fuel combustion and global warming. The third group of multiple
anthropogenic stresses listed in Exhibit 3 result from increasing combustion of fossil fuels,
releasing gases responsible for the greenhouse effect. To date, the potential impacts of
global warming on any of the groups of organisms identified in this report are uncertain,
although warmer than usual temperatures in tropical areas have already been implicated
in the increased incidence and severity of coral bleaching and death worldwide. A more
near-term effect of global warming and deforestation that has not yet received much
attention is the alteration of global and regional weather patterns, resulting in more
extreme temperature and rainfall fluctuations than experienced in the evolutionary
history of the plants and animals native to their locales. Unusually cold weather for a
given season has been blamed for localized kills and population reductions of amphibians
and hatchling turtles, for contributing to the dieback of north temperate forests
weakened by the consequences of atmospheric pollution. Unusually high temperatures
that appear to be responsible for the recent widespread coral bleaching events may
reflect increased variability in weather rather than any actual current manifestation of a
sustained trend towards global warming. Unusual and prolonged recent droughts have
contributed to the loss of wetland and surface water habitat which are contributing to the
declines of duck (and other water bird) populations, and probably contributing to
declines in North American freshwater fish and amphibian populations and increased
incidence of forest dieback in the western United States.
Fossil fuel combustion and acid rain. Combustion of fossil fuels, particularly coal
with high sulfur content, releases gases to the atmosphere that are precursors to acid
deposition. By lowering the pH of surface waters, acid deposition is contributing to the
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decline in North American fish and possibly amphibian populations. Acid deposition
alters soil chemistry (e.g., increased mobility of toxic metals such as aluminum, increased
leaching of essential nutrients from the soil) and is probably a major contributor to forest
dieback in the northeast United States and in parts of Europe.
Introduced species. Human activities have greatly accelerated the introduction of
species into habitats in which they did not evolve. Some introductions have been
intentional, as with stocking rivers and streams with non-native sport fish and introducing
agricultural plants and animals. Others are accidental, as the release of insects travelling
hidden in agricultural produce or marine organisms on ship hulls or in ballast waters.
Introduced species often have no natural predators or other controls in the new
environment. Repeated cases have demonstrated that unchecked generalist species can
often outcompete and replace several more specialized species. The scientific community
considers introduced species to have caused declines in populations of North American
fishes and probably amphibians. There are numerous examples of local island species
extinctions as a consequence of introduced species because long-isolated island
communities are particularly vulnerable to the introduction of generalist species that
evolved in mainland assemblages (e.g., extinctions of native Hawaiian flora and fauna
over the past 500 years). Introduced species are far more difficult to control than habitat
alteration or chemical pollution because they reproduce themselves.
Direct exploitation. Humans have directly reduced animal populations by taking
animals for use as food, pets, research, and exotic trade. Direct exploitation of species
and groups of species has contributed to the declines of North American fish, sea turtles,
and coral reefs and possibly to the declines in amphibians worldwide. Selective logging
of hardwoods is degrading tropical forests. The consequences of overharvesting have
been particularly devastating in the old growth forests of the Pacific Northwest of the
United States and in other groups not covered by this report (e.g., Atlantic and Pacific
coastal fisheries and African and other Old World tropical mammals). Direct taking of
plants and animals can be a self-limiting process if humans perceive a species or
population loss in time to develop sustainable harvest population management
techniques. There are many examples, however, of human failure to check exploitation
in time (e.g., passenger pigeon).
Incidental losses. Human harvesting techniques have sometimes involved the
incidental capture of non-target organisms in large numbers. The shrimping and tuna
industries have long contributed to large kills of sea turtles and dolphins, and use of
dynamite in fishing near coral reefs has contributed to their decline. Kills of adults of
long-lived, low-fecundity16 animals such as sea turtles and dolphins can significantly
reduce the populations' reproductive capacity and ability to recover once incidental kills
are reduced or eliminated.
16Low number of offspring produced each year.
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33. Monitoring Environmental Change
Although we can conclude that several different human activities have contributed
to the observed declines in species and populations of several groups of organisms, the
question still remains to what degree can any one or a number of these groups serve as
indicators of environmental change on regional, national, hemispheric, or global scales.
Each group is sensitive to a somewhat different suite of environmental conditions, and so
each may provide a different window by which to view environmental conditions. One
difficulty with using any of the groups as an indicator of environmental change is
monitoring the group on a sufficiently large scale, with sufficient precision, and over a
long enough period, to detect real trends in the first place. A second difficulty is
monitoring the possible environmental stressors that may contribute to the trends on a
comparable scale and level of precision. There also can be significant time lags between
the occurrence of a stressor and obvious changes in various groups of organisms. Finally,
given the large number of environmental variables involved and natural fluctuations in
environmental conditions (e.g., weather) and population levels, establishing cause and
effect can require a substantial effort with respect to geographic extent of samples,
parameters monitored, and duration of the monitoring programs.
For some of the groups of organisms presented in this report, long-term large-
scale monitoring programs have made it possible to detect population trends despite
large year-to-year and geographic variation in population sizes (e.g., US FWS May
Breeding Waterfowl Survey and Breeding Bird Survey, the Audubon Christmas Bird
Counts). It therefore may be possible to use these groups as sentinels of specific types of
environmental change. Populations of neotropical migrants may serve as barometers for
forest loss and fragmentation in North America and, possibly, the neotropics. Ducks may
serve as a barometer of the condition of some of our North American wetland
ecosystems. In the cases of North American freshwater fish and coral bleaching, efforts
of individual researchers compiling numerous independent studies have identified large-
scale trends, but there is a need to establish a more comprehensive and standardized
approach to monitoring both the populations of concern and the stressors that can be
affecting them. Both North American freshwater fish and coral reef communities are
likely sensitive indicators of change in their environments, integrating a variety of
stressors in their responses. North American freshwater fish are more indicative of gross
habitat-level changes in freshwater ecosystems, whereas coral communities are more
indicative of changes in the quality (e.g., nutrient load, sediments, toxic substances,
salinity, temperature) of the ocean waters.
For the remaining groups of organisms, the utility of the group as a monitor for
environmental change, at least in the short term, is less clear. As yet, it is not clear
whether amphibian species are showing declines worldwide. This results from a lack of
long-term monitoring data for most populations, a problem which the newly established
IUCN Task Force on Declining Amphibian Populations should help to solve. Similarly,
there is a lack of extensive baseline data against which to evaluate trends in land turtles.
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As long as sea turtle juveniles and adults are suffering high mortality rates at sea as a
consequence of shrimp trawling, it will not be possible to use sea turtle populations as
indicators of the quality of ocean waters and the quantity and quality of breeding
beaches. However, the incidence of tumors in sea turtles may provide an indication of
chemical pollution. Dolphins and seals may be sensitive indicators of the accumulation of
toxic substances (e.g., PCBs) in aquatic food chains; however, scientists have not yet
conclusively linked the observed mass mortalities and most declining populations to
environmental contamination.
Monitoring technologies and programs are being established that will allow various
agencies and organizations to follow the areal extent and condition of forests in North
America and worldwide. EPA, through its Environmental Monitoring and Assessment
Program (EMAP), already is cooperating with the USDA Forest Service in the Forest
Health Monitoring (FHM) program in twelve states in the new England, Mid-Atlantic,
and Southeastern regions of the United States. Because of the central role that forests
play in carbon cycling, climate control, provision of wildlife habitat, supply of wood and
other natural products of commercial value, measures of changes in forest area and
condition directly affect the overall health and biological diversity of the planet.
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