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AMER. ZOOL.

, 33:524-536 (1993)

Coral Reefs: Present Problems and Future Concerns


Resulting from Anthropogenic Disturbance'
ROBERT H. RICHMOND
Marine Laboratory, University of Guam, UOG Station, Mangilao, Guam 96923

SYNOPSIS. Coral reefs, with their vast diversity of invertebrate, verte-


brate and algal species, have undoubtedly been subjected to natural dis-
turbance since their appearance millions of years ago. Anthropogenic
disturbance has been a factor affecting reefs for a fraction of that time,
yet in terms of overall impact, may be of greater concern. Data on habitat
destruction, pesticide and heavy metal accumulation, nutrient loading,
sedimentation, runoff and related impacts of man's activities indicate that

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many coastal reefs are endangered by these processes through alterations
in animal-algal symbioses, shifts in competitive interactions, direct mor-
tality, reproductive failure, and insufficient recruitment. The death of
corals critically affects reef communities, as corals provide an important
trophic link as well as the main habitat structure. While natural distur-
bance is an important factor affecting reef interactions, species diversity
and evolution, chronic anthropogenic disturbances combined with unsuit-
able environments for recovery, are of great concern. Physiological stress
can be measured in corals in addition to outright mortality, allowing the
impacts of specific disturbances to be assessed. Sufficient data for distin-
guishing real problems from temporal variability are becoming available,
allowing scientists to focus on practical solutions to problems in coral
reef management and preservation.

INTRODUCTION Coral reefs are unique among high-diver-


Coral reefs are diverse and productive sity and high-productivity marine com-
biological communities which thrive in munities, distinguished by their ability to
shallow and coastal tropical marine envi- thrive in clear, oligotrophic waters devoid
ronments. While scleractinian reef-building of high levels of nutrients. As in temperate
corals are not necessarily the most abundant marine communities, unicellular algae are
or diverse faunal component of coral reefs, responsible for the initial photosynthetic
they provide the initial trophic link through fixation of carbon on coral reefs; however,
their symbiosis with algae and produce the here they reside intracellularly within the
majority of the habitat structure for other endodermal cells of the coral host in a mutu-
reef organisms. Many invertebrate, fish and alistic symbiotic association rather than as
algal species are integral members of a phytoplankton. The relationship between
healthy reef community. By understanding reef-building corals and their symbiotic uni-
trophic relationships and species interac- cellular dinoflagellates ("zooxanthellae") is
tions, we can gain an appreciation for how central to the existence of coral reef com-
coral reefs work, and of critical importance, munities. Metabolites are exchanged
how changes including anthropogenic dis- between the algae and the host, and nutri-
turbance, can affect community structure ents are conserved in an otherwise nutrient
and function. limited environment. Changes in the envi-
ronment which affect the symbiotic asso-
1
ciation {e.g., nutrient levels and light) will
From the Symposium The Crisis in Invertebrate affect coral nutrition, metabolism and cal-
Conservation presented at the Annual Meeting of the cification, and hence, the entire reef com-
American Society of Zoologists and the Canadian Soci-
ety of Zoologists, 27-30 December 1992, at Vancou- munity.
ver, British Columbia. Coral reefs are biogenic structures which
524
ANTHROPOGENIC DISTURBANCE ON CORAL REEFS 525

may form banks, atolls, islands, and sub- nal fertilization or via internal fertilization
stantial masses like the Great Barrier Reef and brooding, is essential for maintaining
of Australia. Living reefs not only form land, reef populations (see reviews by Richmond
but provide the sand that lines tropical and Hunter, 1990 and Harrison and Wal-
beaches, and the structures which buffer lace, 1990). Water and substratum quality
waves that would otherwise cause extensive affect reproduction and recruitment success,
coastal erosion. The protection that reefs and hence, should be the focus of studies
provide islands is especially evident during on long and short term effects of stress and
typhoons and tropical storms where reef disturbance.
crests, reef flats and windward spur-and- The terms "stress" and "disturbance"
groove formations dissipate wave energy have been applied to coral reefs and many
quickly and efficiently. The balance between other biological communities, with a vari-
reef accretion and erosion depends on the ety of interpretations. In this paper, I will

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living veneer of corals and coralline algae. adhere to the concepts suggested by Rosen
The death of key organisms or the shift from (1982) and Brown and Howard (1985) which
an autotrophic to a heterotrophic (suspen- recognize that a gradient of conditions exists,
sion/detritus feeding) community shifts the from ideal to the absolute limits of survival,
dynamics from carbonate deposition to reef and that effects short of mortality need to
erosion. be considered. Stress is a physiological con-
The economic value of coral reefs is evi- dition which results from adverse or exces-
denced by the islands and land they produce sive environmental factors and in corals can
and protect, the fisheries which they sup- be measured by decreased growth rates,
port, the tourists they draw, the recreational metabolic differences, and biochemical
opportunities they afford and the diversity changes. Disturbance is an ecological phe-
of natural products which they produce nomenon which includes departures from a
which have already proven to be of bio- routine set of conditions.
medical importance. While the value of a There are varying levels of degradation
resource is often measured in dollars, one which can be observed on coral reefs, from
should not ignore the cultural value of coral the extreme and obvious (mortality) to more
reefs, which is every bit as important to sublime changes in characteristics including
islanders and tropical coastal populations competitive dominance among organisms,
as the rain forest is to its inhabitants. McAl- decreased growth rates, breakdown of
lister (1988) estimated fisheries losses due organismal associations, reduced fecundity,
to reef degradation at over $80 million per reproductive failure, and declining recruit-
year, impacting 127,000 jobs and 637,000 ment of larvae. Essentially, whether a coral
family members. Finally, coral reefs are reef is killed in a week, due to sediment
simply beautiful, and that may be reason burial, or over a ten year period, due to
enough to warrant their protection. attrition and lack of recruitment, the result
Coral reef organisms are usually consid- is the same: the loss of the coral reef com-
ered stenotypic, exhibiting a relatively nar- munity and all of the benefits which it offers.
row range of tolerances to environmental The two plenary presentations at the Sev-
conditions, hence small changes in environ- enth International Coral Reef Symposium
mental quality can affect critical biological (Guam, 1992) focused on world-wide
processes. Reproduction and recruitment are destruction of coral reefs in the face of
the two processes by which reef populations increasing pressure from man's burgeoning
are maintained, and both can be quantita- populations, indicating an awareness among
tively assessed, allowing determination of coral reef scientists that anthropogenic (man-
sublethal effects of environmental changes. induced) disturbance is a critical problem
While corals and many other reef inverte- (Buddemeier, 1993; Wilkinson, 1993).
brates are capable of asexual reproduction As this paper was prepared for a sym-
(fragmentation, tissue sloughing and regen- posium entitled "The crisis in invertebrate
eration), successful production of larvae, conservation," the focus will be on the effects
either through release of gametes with exter- of disturbance on coral reefs, and specifi-
526 ROBERT H. RICHMOND

cally, with concerns for the health of reefs reported decreased coral growth rates
in the face of mounting pressure from man's resulting from decreased light levels avail-
activities. The range of activities which are able to corals due to sedimentation from
cause for concern includes runoff and sed- dredging. Rinkevich (1989) found that plan-
imentation from development projects, ula production in Stylophora pistillata is
eutrophication from sewage and agriculture, energetically supported by metabolites
physical impact from maritime activities, translocated from symbiotic zooxanthellae,
dredging, collecting and destructive fishing linking photosynthesis to reproduction in
practices, pollution from industrial sources, corals. Other studies (see reviews by Brown
golf courses and oil refineries, and the syn- and Howard, 1985 and Rogers, 1990) have
ergistic impacts of anthropogenic distur- also shown that decreased light levels have
bance on top of natural disturbance. a detrimental effect on corals, and can limit
Some coral researchers have argued that the depth range over which corals can exist.

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natural disturbances such as El-Nino events Physically, sediments also interfere with
and typhoons have historically devastated coral nutrition by coating the feeding sur-
vast stretches of coral reefs, and that by faces responsible for catching prey items
comparison, documented anthropogenic needed to supplement the energy provided
reef loss has been smaller in scale and of by zooxanthellae. While corals do have the
indeterminate long-term consequences. For ability to cleanse themselves using a com-
example, Grigg and Dollar (1990) recognize bination of mucus secretion and ciliary
the seriousness of damage to local reefs from action, chronic sedimentation may exact a
human activities, but they remain uncon- high energetic cost, adding to the overall
vinced that anthropogenic disturbances are impact on the colony. Sedimentation can
as serious or pervasive as natural distur- alter species composition of reefs through
bances. I disagree with arguments that photosynthetic and physical effects. Changes
downplay the importance of anthropogenic in relative abundance of morphological types
disturbance because: 1) we cannot control as well as individual species are an impor-
nature but we can control human impacts; tant reflection of how sedimentation as a
2) differences do exist between the effects of disturbance affects community structure.
natural and anthropogenic disturbance; and Sediments can also physically interfere
3) the synergistic effects of anthropogenic with recruitment of coral larvae, which
disturbance on top of natural disturbance require a solid substratum upon which to
change the conditions for recovery. This settle and metamorphose. Te (1992a) found
paper addresses the most common types of tissue from newly settled and calcifying col-
anthropogenic impacts on coral reefs, onies ofPodllopora damicornis "bailed out"
important differences between types of dis- of their benthic exoskeleton in response to
turbance, summarizes the results of some increased sedimentation, which is a previ-
previous studies, and offers some ideas on ously described stress response (Sammarco,
mitigation measures as well as future areas 1982; Richmond, 1985). Dredging projects
of research. have been particularly damaging to reefs,
IMPACTS ON CORAL REEFS
primarily through the initial physical dis-
turbance, habitat alteration and the subse-
Sedimentation quent problems associated with sedimen-
Sedimentation, which is the most well- tation.
studied impact, may affect corals three dif- Few studies have focused on the chemical
ferent ways: photosynthetically, physically, effects of sediment on corals, which can be
and chemically. As most reef-building cor- important. Brown and Holley (1982) and
als obtain the majority of their nutritional Howard and Brown (1984) studied the
requirements via translocation of metabo- effects of heavy metals (copper, tin and zinc
lites from their photosynthetic partners compounds) on adult coral colonies, with
(Muscatine et ai, 1981), any reduction in mixed results. Goh (1991) determined low
the available quality and/or quantity of light levels (9 ppm) of nickel caused mortality in
will affect coral nutrition, growth, repro- coral planulae and significantly reduced lar-
duction and depth distribution. Bak (1978) val settlement rates at concentrations of 1
ANTHROPOGENIC DISTURBANCE ON CORAL REEFS 527

ppm. Several studies in Okinawa, Japan, performed found chemicals assayed for were
have found that lateritic soils (red clay, high in quantities below detectable limits." This
in iron), have been particularly detrimental says nothing about the effects of the chem-
to reef corals compared to carbonate sedi- ical component of runoff on the local flora
ments (Nishihira, 1987; Yamazato, 1987; and fauna. Bioassays are the appropriate
Sakai et al, 1989). tests to be performed, and should be required
An aspect of the chemical effects of sed- before permits are approved. Recent
iment on coral reefs has not yet been advances in our understanding of inverte-
addressed: How do chemically treated soils brate reproduction in general and settle-
deposited on coral reefs affect resident ment and metamorphosis of benthic inver-
organisms? Golf course construction on tebrate larvae in particular demonstrate the
tropical islands has increased at an alarming reasons for concern.
rate in the past few years, considering the Most scleractinian corals are simulta-
size of the land masses involved, the quan- neous hermaphrodites (containing both male

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tities of pesticides and fertilizers used, and and female gonads at the same time) which
the fresh water requirements for maintain- participate in discrete annual multispecies
ing greens and fairways. If the pesticides spawning events (Richmond and Hunter,
used bind to the soil, and the soil ends up 1990; Harrison and Wallace, 1990). For
on the reef due to erosion, the question of Guam and Okinawa, the timing of mass
chemical impacts needs to be addressed. coral spawning events coincides with the
Clay particles, which by their small size will height of the rainy season, when coastal
often be carried to the ocean by runoff, have marine surface waters are most likely to be
a charge which may change when entering contaminated from terrigenous runoff.
the marine environment. Chemicals bound During the summers of 1989, 1990, and
to particles on land may be released in sea- 1991 coral fertilization bioassays were per-
water. Experiments with the organophos- formed comparing fertilization and devel-
phate pesticide Dursban (chlorpyrifos) found opment success of gametes and embryos,
seawater passed through a column of soil respectively, among waters of differing
treated with a quantity of chemical equal to salinity and sediment content. In one exper-
that applied to golf courses, was toxic to the iment performed using water samples col-
coral Pocillopora damicornis (Te, 19926). lected on the night of coral spawning above
Acevedo (1991) determined chlorpyrifos at a reef adjacent to a stream mouth in Oki-
levels of 1 ppm resulted in up to 50% mor- nawa, runoff was found to cause an initial
tality in assays with coral planulae. Bioas- 53% drop in fertilization rate compared to
says like these indicate the need for more a control, and an additional 51% drop in
such studies. the number of embryos developing to the
planula larva stage (Richmond, unpub-
RUNOFF/CHEMICAL POLLUTION/WATER lished). The experimental treatment sea-
QUALITY water was determined to have a salinity of
A general rule for islands: Whatever is 28.5%o, with suspended solids (red clay) of
used on land today ends up in the aquifer 1.28 g/liter, while the control water was Mil-
or coastal zone tomorrow. While sediment lipore filtered (0.45 Mm) and had a salinity
carried by runoff has been a major focus of of 34.4%o.
environmental studies, little attention has Since no additional chemical analyses
been paid to the chemistry of runoff water. were performed on the runoff-affected sea-
Salinity changes alone have proven to affect water, it was not possible to determine if
corals, especially on shallow water reef flats other substances were responsible for the
which are most likely to be impacted by 77% drop in larval production compared to
freshwater runoff (Kato, 1987; Jokiel et al., the control. A subsequent experiment to
1993). What are the specific concerns that determine the effects of decreased salinity
need to be addressed? alone showed an 86% reduction in fertiliza-
Having reviewed numerous environmen- tion rate accompanying a 20% dilution of
tal impact statements (EISs), water quality seawater with distilled water. These exper-
reports on runoff usually read "all analyses iments demonstrated that actual coastal
528 ROBERT H. RICHMOND

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FIG. 1. Sediment plume off Southern Guam. Corals up to several hundred years old were killed by sediment
burial. Water samples from plumes like this were found to cause up to an 86% drop in fertilization rates in
spawning corals. The plume is ca. 1 km in diameter.

surface water quality above reefs during coral events which should be addressed sepa-
spawning events was sufficiently reduced to rately (Hadfield and Pennington, 1990;
cause reproductive failure. Considering most Pawlik and Hadfield, 1990). While larvae
coral species spawn once a year, during the of benthic organisms may settle out of the
rainy season when coastal pollution would plankton and come in contact with the sub-
be expected to reach its peak, and that most stratum, metamorphosis may not occur
coral eggs are buoyant, floating in the sur- without chemosensory recognition of spe-
face water layer for up to several hours before cific inducing molecules (Morse, 1990). The
fertilization occurs, it is easy to see the link concentrations of metamorphic inducers in
between terrigenous runoff and reproduc- nature are far below detectable limits based
tive failure of spawning reef species. Fur- on present technology, yet are obviously in
thermore, chemical cues have been found sufficient quantities in the marine environ-
to allow synchronization of spawning in ment to affect metamorphosis (10~10 M for
corals (Atkinson and Atkinson, 1992; Rich- the nudibranch Phestilla sibogae, Hadfield
mond, unpublished). Decreased water qual- and Pennington, 1990). Pollutants below the
ity could also affect these critical cues, pre- detectable limits of high performance liquid
venting synchronous release of gametes and chromatography (HPLC) are not necessarily
resulting in lowered reproductive success. below the limits of interfering with critical
Suppose spawning occurs in a pristine chemical cues in marine invertebrates.
environment, allowing fertilization and Guam's southern reefs provide an exam-
embryological development to occur at nat- ple of how water quality impacts coral reefs
ural rates. Can fully developed planula lar- through sublethal effects. During the period
vae settle in areas of reduced water quality? from 1988-90, a major road construction
Recent discussions of larval recruitment in project was undertaken on southern Guam,
benthic invertebrates have suggested that which is geologically volcanic with steeply
settlement and metamorphosis are different sloping, highly erodible lateritic soils. Large
ANTHROPOGENIC DISTURBANCE ON CORAL REEFS 529

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FIG. 2. Coastal reef off Southern Guam which was killed by sedimentation. A fairly dry typhoon removed
sediment accumulations from the reef.

quantities of sediment ladened freshwater ure on nearby and distant reefs. Considering
runoff impinged on coastal reefs, causing coral planulae remain competent (able to
high levels of coral mortality, rapid growth successfully settle and metamorphose) for
of fleshy algal species, and large parcels of periods from days to months (Richmond,
reduced salinity/quality seawater (Figs. 1- 1987, 1988), a regional view of coral reef
4). Local fishermen have complained of population dynamics is needed. Reproduc-
decreased fisheries and reef vitality not only tive failure in one area may affect recruit-
on these coastal reefs, but also on offshore ment elsewhere. Numerous genetic studies
islands and reefs not directly impacted by have shown gene flow among populations
contact with the sediment. Inspection of of marine invertebrates. The significance of
these reefs revealed live adult coral colonies, environmental degradation in one area on
but no signs of larval recruits for the period recruitment in another should not be
coinciding with and following construction ignored.
activities and increased levels of sedimen- Oil pollution is an extreme example of
tation and runoff. how chemicals, in this case hydrocarbons,
In contrast, surveys of Kossol Reef, can impact reefs. Research performed in the
Republic of Palau, performed in September, Gulf of Eilat has documented coral mor-
1992, revealed up to 12 coral larval recruits tality, decreased fecundity and recruitment
per square meter in an area devastated by failure in response to chronic oil pollution
a typhoon in 1989. Coral recruits could be (Fishelson, 1973; Loya, 1975, 1976; Loya
identified from each of the year classes since and Rinkevich, 1979; 1980). Chemical fish-
1989, including small colonies resulting ing techniques including the use of cyanide
from the 1992 summer spawning. The point for collecting aquarium fish and chlorine
is, while levels of stress may be sublethal to bleach for consumptive fishing have also
adult coral colonies, they may be sufficient had a negative impact on reefs in the Phil-
to cause reproductive and recruitment fail- ippines and Micronesia.
530 ROBERT H. RICHMOND

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FIG. 3. Porites colony being overgrown by algae.

Water quality is a critical consideration and increased mortality from bacterial


in understanding anthropogenic impacts on infection (Smith et al, 1981; Pastorok and
coral reef communities, especially in how Bilyard, 1985; Tomascik and Sander, 1987).
pollutants affect egg-sperm interactions and Corals are adapted to live in nutrient poor
chemosensory cues critical to reproductive environments (Muscatine and Porter, 1977),
synchrony, fertilization success, larval set- and are relatively slow-growing compared
tlement, metamorphosis and recruitment. to algae, sponges, tunicates and other groups
of sessile, benthic organisms. Nutrients not
SEWAGE only increase the biomass of phytoplankton,
The effects of sewage on coral reefs, affecting light transmission and increasing
reviewed by Pastorok and Bilyard (1985), the biochemical oxygen demand (B.O.D.)
result from several factors including nutri- to the point that corals may be impacted
ents, sediment (suspended solids) and toxic (Guzman et al., 1990), but also give a com-
substances. The overall impact of sewage petitive advantage to faster growing benthic
on a coral reef community depends on site- species. The green algae Dictyosphaeria cav-
specific conditions including volume of ernosa, formed large mats, covering and
sewage, level of treatment, presence of toxic killing corals in Kaneohe Bay, Hawaii, due
materials, and receiving water characteris- to sewage pollution (Smith et al., 1981;
tics. Evans et al., 1986). Additionally, portions
The effects of sewage-related nutrient of the Kaneohe Bay community shifted from
enrichment on coral reef communities have a coral-dominated autotrophic community
been documented, and include alteration of to an algae-dominated suspension feeding
competitive interactions, reduction of coral community because of eutrophication. Spe-
calcification rates from decreased light lev- cies of sabellid and serpulid worms and other
els and increased phosphate concentrations, boring organisms thrived during the period
ANTHROPOGENIC DISTURBANCE ON CORAL REEFS 531

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FIG. 4. Nutrient input caused an increase infleshyalgae biomass, which is now binding the sediment, preventing
normal turbulence from cleansing the reef of accumulated sediment.

of sewage input, eroding the carbonate age suspended solids are primarily organic,
structure of the reefs and undermining the can contain adsorbed toxins, and increase
base upon which coral recolonization took B.O.D. more than inorganic sediment asso-
place following sewage diversion. ciated with runoff. The toxic component of
Dubinsky et al. (1990) have also dem- sewage depends on the sources of input, and
onstrated that nutrient enrichment via sew- is primarily a concern in industrial or agri-
age reduces the photosynthetic efficiency of cultural areas where industrial wastes and
corals, as algal cells increase in density to pesticides are included in the effluent.
the point of becoming self-shading. Since
the coral-zooxanthellae symbiosis evolved TEMPERATURE STRESS
under nutrient limited conditions, it is rea- The negative impacts of increased tem-
sonable to assume that the relationship will perature on corals have been documented
become altered in response to changes in from both anthropogenic and natural
the level of nutrients available. Further sources. Jokiel and Coles (1974) found coral
studies of the physiological effects of such mortality associated with the heated ther-
changes are needed to determine the sub- mal discharge from a cooling system for a
lethal or long-term effects of sewage and power plant in Hawaii. Glynn (1990)
nutrient enrichment on coral reefs. reported widespread coral mortality in the
While the effects of suspended solids from eastern Pacific associated with increased
sewer outfalls have been compared to those temperatures accompanying the 1982-83 El
from terrigenous runoff and sedimentation, Nino event. In both cases the cause of mor-
the two types of sediment differ in physical, tality appeared to be the breakdown of the
chemical and toxicological characteristics, symbiotic association between the zooxan-
which must be considered when assessing thellae and the coral host (bleaching). An
impacts (Pastorok and Bilyard, 1985). Sew- important distinction between the two
532 ROBERT H. RICHMOND

sources of stress is duration. Studies follow- oping Pacific Islands as potential sites for
ing the two examples presented here found disposing of toxic wastes. In 1990, a pro-
corals recovering after the temperature stress posal from an Australian company was sub-
was removed, indicating corals can rebound mitted to the Government of Palau for the
from acute temperature disturbances. The construction of a toxic waste disposal incin-
1982-83 El Nino ended naturally, but it took erator/power plant. Among the materials
redesigning and rebuilding the power plant listed as suitable to be used as fuel to pro-
outfall before recovery occurred at the duce electricity were coal tailings, sewage
Hawaii site. sludge, dioxins, lead, sulphur, and cyanide
contaminated wastes, PCBs, and heavy
CORAL BLEACHING metal liquors (Graves, 1992; Lohning
Widespread coral bleaching (loss of zoo- Brothers, 1990). In 1992, the U.S. Securities
xanthellae) has been observed in both the and Exchange Commission suspended trad-
Atlantic and Pacific oceans, and has been ing of stock in a company called Pacific

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linked to unusually high temperatures and Waste Management Inc., which was pro-
irradiance (Williams and Williams, 1988; moting the development of the toxic waste
Williams et al., 1987). This topic is reviewed incinerator in Palau, noting concerns
in a special issue of the journal Coral Reefs including several name changes of the com-
(vol. 8, no. 4, 1990), which presents dis- pany, and that the Palau constitution has a
cussions of both natural and anthropogenic provision banning the importation of toxic
sources of temperature increase. The rela- matter (Graves, 1992; North, 1992).
tionship between bleaching events and ozone In December, 1992, a barge containing
depletion/global warming is presently being 5,200 tons of petroleum contaminated soil
studied by several groups of researchers transited Guam en route to the Marshall
(Buddemeier, 1993). If the connection can Islands, where the material was to be used
be proven, it will be an example of global in construction of a causeway between two
rather than local anthropogenic impacts on islands in Kwajalein Atoll (Brooks, 1992a,
coral reefs. b; Glauberman, 1993). Concerns about the
environmental acceptability of the pro-
CORAL DISEASES posed activity resulted in the fully-loaded
Four types of coral diseases have been barge returning to its point of origin in
"identified": white band disease, black band Honolulu, Hawaii, where alternate means
disease, bacterial infection, and shut-down of disposal are being considered.
reaction (Antonius, 1981). While there is a The costs of handling and disposing of
degree of uncertainty as to the causes toxic materials are high, and islands in need
responsible for each disease, they all appear of income, and without adequate techno-
to be stress-related. This is one area where logical expertise, are attractive opportuni-
synergisms are believed to play an impor- ties for getting rid of such wastes at minimal
tant role, as stressed corals seem to be the costs. I believe this situation remains an
most susceptible. Tumors, bacterial attack important concern for Pacific coral reefs. As
and parasitic worms have been observed in with pesticide runoff, the problem may be
areas where corals have been stressed by with long-term effects, bioaccumulation of
sediment, sewage, pesticides, heavy metals substances by organisms and the results of
and other human impacts (Mitchell and chronic exposure.
Chet, 1975; Brown and Howard, 1985;
Glynn et al., 1989; C. Hunter, personal DESTRUCTIVE FISHING PRACTICES
communication). The use of dynamite and poisons, includ-
ing chlorox and cyanide, have been respon-
Toxic WASTE sible for the destruction of coral reefs
Within the last few years, a new threat throughout the world. Because of the size
has emerged, endangering the health of cor- of the areas concerned, and the general lack
al reefs of the Pacific Islands. Several com- of resources for enforcement, education
panies have been targeting cash-poor devel- appears to be more successful than legisla-
ANTHROPOGENIC DISTURBANCE ON CORAL REEFS 533

tion in controlling these practices. Poverty an increasing number and/or the persistence
reduces the alternatives for fishermen who of these events may be linked to anthro-
must feed their families and rely on fishing pogenic nutrient input.
as a source of protein and income. This same
problem has lead to another anthropogenic
DISCUSSION
disturbance on reefs: overfishing. The use
of fish traps made of long-lasting materials Anthropogenic versus natural disturbance
with small mesh sizes results in the capture This is certainly not the first discussion
of pre-reproductive juveniles, affecting or comparison of anthropogenic versus nat-
future populations, and the death of fish ural disturbance, nor will it be the last. As
when traps become dislodged during storms, scientists, we often look for trends, gener-
yet continue to capture fish which eventu- alizations and rules, perhaps even where
ally starve. Several types of net fishing have such things are not appropriate. It is easy
also been responsible for over-exploitation to pick specific examples which support

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of reef resources as well as impact damage either side of the debate: 1) that there is little
to coral reefs. As with all biological com- qualitative difference between anthropo-
munities, each species plays an important genic and natural disturbance to coral reefs
role in the dynamics of balance. The deple- (Grigg and Dollar, 1990), and 2) that impor-
tion of grazers, for example, may eventually tant differences do exist, which affect recov-
lead to an overgrowth of algae. While it is ery, mitigation and management decisions
simple to prove how damaging destructive (Johannes, 1975; Loya, 1976). For example,
fishing practices are to the productivity of Grigg and Dollar (1990) report the impact
fisheries, the economic realities of day-to- of a kaolin spill on French Frigate Shoal,
day life on some tropical islands makes the Hawaii, was trivial, yet tropical storms cause
solution difficult to obtain. catastrophic coral mortality. The stress on
French Frigate Shoal was acute, kaolin is
CROWN-OF-THORNS STARFISH inert, non-toxic with no B.O.D., and the site
The coral-eating starfish, Acanthaster is an area with high water motion, far
plancii, has been the focus of a debate on removed from any other chronic sources of
the fate of coral reefs since major outbreaks pollution. Had the same spill occurred in a
were observed in the late 1960s and early harbor, or on a coastal reef adjacent to a
1970s (reviewed in a special issue of the populated area, the long-term impact would
have been much greater, especially due to
journal Coral Reefs, vol. 9, no. 3, 1990). synergisms and continued interference with
While it has been documented that hun- recovery and recruitment. As far as effects
dreds of km2 of coral reefs have been dev- of tropical storms and typhoons, while the
astated by population blooms of the starfish, overall appearance could be described as
the debate centers on whether the outbreaks catastrophic, such events usually crop the
are natural events, having occurred repeat- reef rather than completely kill the corals.
edly over geologic time, or if the situation One of my primary collecting sites for stud-
has arisen as a result of man's activities. ies of coral reproduction is the windward,
Although sediment core data have indicated exposed reef behind the University of Guam
Acanthaster outbreaks occurred 10,000 years Marine Laboratory. During the past seven
ago, recent studies have shown a relation- years, there have been at least eight major
ship between nutrient input and recruit- typhoons, during which wave wash has
ment success of the larvae (Birkeland, 1982). reached as high as 33 feet above sea level.
Studies of echinoderm reproduction have There has not been a single year that I have
demonstrated that the success of recruit- not been able to collect a variety of gravid
ment of their planktotrophic larvae depends corals from this site.
on phytoplankton availability following
spawning. Events that increase nutrient When defending projects or activities
availability on coral reefs can affect repro- potentially harmful to coral reefs, paid con-
duction and recruitment in Acanthaster. sultants often argue that if there are no data
While outbreaks may be considered natural, that prove the proposed activity is detri-
534 ROBERT H. RICHMOND

mental, the project or activity should be eries thrive on nutrient input, coral reefs
allowed. This sets the stage for classical type suffer whenever water clarity goes down and/
II statistical error: accepting a false hypoth- or nutrient levels go up. Better erosion con-
esis. Simply put: the absence of data show- trol standards, increased retention of fresh-
ing harm often indicates a lack of data rather water on land, and diversion of sewage to
than no effect. When adequate and accurate areas which carry the material away from
data demonstrate no detrimental effects, reefs are all solutions which can readily be
then and only then should projects be applied.
approved. Globally, coral reef preserves are criti-
Data summarized in this paper support cally needed to serve as refuges for corals
the hypothesis that most chronic distur- and other reef organisms (Buddemeier,
bances are more damaging than acute dis- 1993). Wilkinson (1993) estimates 70% of
turbances, especially when considering coral the world's coral reefs are already seriously
reef recovery. Anthropogenic disturbances, degraded (10%), in a critical state of being

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like runoff, sedimentation, sewage outfalls, lost within the next 10-20 years (30%), or
and oil pollution are characteristically threatened to disappear within the next 20-
chronic perturbances. They generally cause 40 years (30%), leaving an estimated 30%
problems not only by inducing coral mor- as stable, and capable of surviving from
tality, but by affecting reproduction and hundreds to thousands of years. More data
recruitment, and hence, recovery. If such and studies, especially in forms and forums
problems can be controlled, limiting them available and comprehensible to the general
to more episodic and acute disturbances, or public and decision makers are needed if
removing the stress altogether, reefs can, and present trends are to be reversed.
will recover. Perhaps that is the message of In conclusion, acute, natural disturbances
value we can extract from impact studies. are critical to maintenance of diversity on
Corals in Kaneohe Bay, Oahu, Hawaii, did reefs (Connell, 1978), and in the case of
recover from both fresh water kills and tropical storms and typhoons, may actually
eutrophication when sewage input was serve to reduce anthropogenic disturbance
diverted elsewhere (Evans et al., 1986; Hol- by removing accumulated sediments depos-
thus et al., 1986; Jokiel et al., 1993). ited by erosion and sedimentation. Char-
Devastating events normally considered acteristically chronic, anthropogenic distur-
as natural, like Acanthaster outbreaks bance, while often sublethal, and hence,
(Endean, 1973) and red tides (Guzman et more difficult to assess on the short term,
al., 1990), have been found to have links to can cause more serious damage by pre-
human activities increasing runoff and venting recovery while acting to weaken
eutrophication (Birkeland, 1982). Recovery corals and other reef organisms to the point
of Jamaican reefs following Hurricane Allen of eventual mortality. We cannot control
(Woodley et al., 1981) appears to have been nature, but with adequate and accurate data,
impaired by anthropogenic impacts of over- can make decisions which control the
fishing herbivorous fishes and terrigenous impacts of man's activities on coral reef
runoff coincident with the loss of grazing communities.
urchins by disease. This further emphasizes
ACKNOWLEDGMENTS
the types of synergistic interactions that can
occur, affecting the extent of mortality as The author gratefully acknowledges Dr.
well as the possibilities for recovery (Pear- M. G. Hadfield for the invitation to partic-
son, 1981). ipate in this symposium, and for his many
One solution which would drastically helpful comments and Drs. C. E. Birkeland,
reduce the amount of anthropogenic dis- P. W. Glynn, P. L. Jokiel, R. A. Kinzie, III,
turbance on coastal coral reefs is to change D.A. Krupp, and K. Yamazato for numer-
the common engineering practice of using ous discussions on the subject matter of this
the coastal zone as a dumping ground for paper and critical comments. Support for
storm drainage, runoff and sewage.While research included in this paper was pro-
temperate marine environments and fish- vided by NIH/MBRS Grant #53-LA-61158-
ANTHROPOGENIC DISTURBANCE ON CORAL REEFS 535

511, NSF grant BSR 8813350 and a coop- to coral reefs in the tropical eastern Pacific. In P.
erative research support grant from the W. Glynn (ed.), Global ecological consequences of
the 1982-83 El Nino-southern oscillation, pp. 55-
Ministry of Science, Education and Culture 117. Elsevier Science Publishers, Amsterdam.
of Japan to K. Yamazato. This is contri- Glynn, P. W., A. M. Szmant, E. F. Corcoran, and S.
bution number 333 of the University of V. Cofer-Shabica. 1989. Condition of coral reef
Guam Marine Laboratory. cnidarians from the northern Florida reef tract:
Pesticides, heavy metals, and histopathological
examination. Mar. Pollut. Bull. 20:568-576.
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