Identifying Ecological Change and Its Causes: A Case Study On Coral Reefs

Ecological Applications, 14(5), 2004, pp.
14481465
q 2004 by the Ecological Society of America
IDENTIFYING ECOLOGICAL CHANGE AND ITS CAUSES:

A CASE STUDY ON CORAL REEFS
KATHARINA E. FABRICIUS1
AND
GLENN DEATH
Australian Institute of Marine Science, PMB No. 3, Townsville MC, Qld 4810, Australia
Abstract. The successful management of ecosystems depends on early detection of

change and identification of factors causing such change. Determination of change and
causality in ecosystems is difficult, both philosophically and practically, and these difficulties increase with the scale and complexity of ecosystems. Management also depends
on the communication of scientific results to the broader public, and this can fail if the
evidence of change and causality is not synthesized in a transparent manner. We developed
a framework to address these problems when assessing the effects of agricultural runoff
on coral reefs of the Australian Great Barrier Reef (GBR). The framework is based on
improved methods of statistical estimation (rejecting the use of statistical tests to detect
change), and the use of epidemiological causal criteria that are both scientifically rigorous
and understood by nonspecialists. Many inshore reefs of the GBR are exposed to terrestrial
runoff from agriculture. However, detecting change and attributing it to the increasing loads
of nutrients, sediments, and pesticides is complicated by the large spatial scale, presence
of additional disturbances, and lack of historical data. Three groups of ecological attributes,
namely, benthos cover, octocoral richness, and community structure, were used to discriminate between potential causes of change. Ecological surveys were conducted along water
quality gradients in two regions: one that receives river flood plumes from agricultural
areas and one exposed to runoff from catchments with little or no agriculture. The surveys
showed increasing macroalgal cover and decreasing octocoral biodiversity along the gradients within each of the regions, and low hard coral and octocoral cover in the region
exposed to terrestrial runoff. Effects were strong and ecologically relevant, occurred independently in different populations, agreed with known biological facts of organism responses to pollution, and were consistent with pollution effects found in other parts of the
world. The framework enabled us to maximize the information derived from observational
data and other sources, weigh the evidence of changes across potential causes, make decisions in a coherent and transparent manner, and communicate information and conclusions
to the broader public. The framework is applicable to a wide range of ecological assessments.
Key words: Bayesian analysis; biodiversity; bootstrap; causality; community structure; environmental impact; epidemiology; Great Barrier Reef; model averaging; model selection; pollution; terrestrial runoff.
INTRODUCTION
Early detection of ecological change and identification of factors causing such change are essential for
successful ecosystem management. Despite the availability of the best scientific data, interested parties often
disagree about the existence of ecological change and
its causes. There are many reasons for this, including
(1) the selective use of scientific data and other information by interested parties to support individual
claims and objectives, (2) the misinterpretation and
abuse of technical concepts such as probability and
causality (Newman and Evans 2002), (3) the complexities of large-scale ecosystems which cannot be simply
explained or reliably predicted, and (4) the exploitation
of disagreement amongst scientists by stakeholders.
The resulting lack of consensus can lead successively
Manuscript received 15 October 2003; accepted 23 February
2004. Corresponding Editor: P. K. Dayton.
1 E-mail: k.fabricius@aims.gov.au
to conflict, confusion over policy development, government inaction and environmental degradation.
To overcome these problems, we developed a framework based on (1) the use of improved methods for
determining change through estimation of effect sizes,
as opposed to the usual use of hypothesis tests
(McCullagh and Nelder 1989, Nelder 1999), and (2)
the use of epidemiological criteria to attribute causality.
The framework can synthesize and evaluate scientific
and other data according to criteria that are both scientifically rigorous and widely accepted. Application
of the framework is simple and transparent in order to
effectively communicate scientific evidence to decision
makers and the public. This enables the detection of
change and judgments about causality to be made in a
rigorous, structured, and open manner, and thus the
agreement among stakeholders, necessary for successful implementation of management strategies, can be
obtained. An application of the framework follows in
a case study on the effects of water pollution on coral
reef benthos in the Great Barrier Reef, Australia.
1448
October 2004
IDENTIFYING ECOLOGICAL CHANGE AND CAUSE
Statistical issues in the detection of change

The statistical significance test does not tell us what
we want to know, and we so much want to know
what we want to know that, out of desperation, we
nevertheless believe that it does!
Cohen (1994)
Most studies of environmental change (or impacts)
adopt a falsification perspective; that is, they assume
no change has occurred and assess the level of evidence
against this premise. If the evidence against no
change is strong, then they accept change has occurred, whereas if the evidence against no change
is weak, then the initial position is retained. Evidence
against the null hypothesis is almost invariably based
on a frequentist statistical significance test of a point
(precise) null hypothesis. Since ecosystems are constantly changing through time and space such hypotheses are a priori false; i.e., they are not plausible (Berger and Sellke 1987). Despite the no change premise
seeming indefensible, the majority of studies continue
to adopt it as a starting point for investigations of temporal and spatial change. Why is this so? As a basis
for management decisions, hypothesis tests are inadequate, and it can be argued that decision-making
should not be a part of impact studies, which should
inform, not decide (Stewart-Oaten 1996a). Even when
a point null hypothesis is plausible, frequentist tests
are problematic (Berger and Sellke 1987, Berger et al.
1997). They are remarkably uninformative (reject
or fail to reject) and can be misleading when improperly interpreted, e.g., by describing a failure to
reject as evidence of no change or by misinterpretation of P values. Such misunderstandings and the
repeated use of tests of low power can also lead to
false knowledge as the null hypothesis becomes accepted as knowledge. Basing decisions on the result of
tests also conflicts with the precautionary principle
(Bodansky 1991) and can be hazardous, e.g., requiring
a positive test as evidence of population decline for a
rare species with high natural variation can lead to local
extinction. The problem of lack of information as basis
for accepting the null hypothesis has led to the proposal
for reversing the burden of proof (Dayton 1998), e.g.,
it must be shown that proposed actions will not result
in environmental damage, rather than allowing all actions which cannot be shown to result in damage. Frequentists have argued that power analysis (typically
post hoc) offers protection against this problem (e.g.,
Cohen 1988). However, this approach has been criticized, and equivalence testing suggested as a formal
alternative (Hoenig and Heisey 2001). Despite such
shortcomings of frequentist hypothesis tests being repeatedly noted (Berger and Sellke 1987, Raftery 1995,
Stewart-Oaten 1996a, Johnson 1999), the use of tests
still prevails. Various alternatives have been suggested,
primarily through the use of estimation of parameters
1449
with confidence [credibility] intervals (Stewart-Oaten

1996a, Burnham and Anderson 1998, Burnham et al.
2000) or Bayesian methods (Ellison 1996, Berger et
al. 1997, Berger and Pericchi 2001). By abandoning
hypothesis tests in studies of change, immense benefit
can be derived, irrespective of whether frequentist or
Bayesian methods are used. The principal objective
then becomes one of how to quantify (model) change
and obtain accurate estimates of parameters representing the quantities of interest.
When testing for significance or estimating the magnitude of change, typically one or more parameters of
a chosen model represent the change process. It is often
forgotten, or not realized, that all inference, be it hypothesis tests or parameter estimation, is conditional
on the selected model. Thus, the validity of conclusions
based on results of significance tests and parameter
estimates are always contingent on the model being an
accurate representation of reality, i.e., that the model
is true, or is at least a good approximation. Often,
many models are compared before one is chosen, but
the uncertainty involved in model selection is seldom
taken into account (Burnham and Anderson 1998), and
this can result in biased and/or over-precise estimates,
and probability values from hypothesis tests that are
too small. In well-designed experiments or surveys, the
model is largely determined by the study design, and
we can be relatively confident that it is a reasonable
representation of reality. However, when studies are
not as well controlled, or many variables are involved,
then the choices of model can be vast. This further
increases if we consider interactions, transformations
of variables, and alternative error structures. If all possible explanatory variables are included in a model, the
power to detect change (equivalently, the precision of
the estimate of change) may be severely reduced. Conversely, if important variables are omitted, then estimates of change are likely to be biased. The problems
of model selection are particularly difficult for small
sample sizes with weak relationships between the response(s) and predictors, and large data sets with many
predictors.
The use of hypothesis tests for model selection has
received intense scrutiny in recent times, and based on
simulations, the use of tests has been shown to be suboptimal for identifying true models (Freedman 1983,
Draper 1995, Burnham and Anderson 1998). The use
of selection criteria such as Akaikes information criteria (AIC; Sakamoto et al. 1986, Bozdogan 1987) and
Bayes information criteria (BIC; Schwarz 1978, Madigan and Raftery 1994) have been advocated, particularly in the ecological literature (Burnham and Anderson 1998). These criteria outperform the use of hypothesis tests in determining true models, however no
single criteria will universally find the true or best approximating model. Based on AIC or BIC, weights of
evidence can be calculated for each of the competing
models. These weights quantify the uncertainty of mod-
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KATHARINA E. FABRICIUS AND GLENN DEATH
el selection and can be treated as relative probabilities

of the models. They do not, however, represent the
probability that any particular model is the true model,
or best approximating model of all possible models,
since all of the proposed models may be deficient. If
none of the models are true (or good approximations),
then inferences based on the best model are also likely
to be biased.
One way to overcome the issue of choosing a single
model is simply to avoid it by model averaging. This
also has the attractive property of generating more accurate estimates and predictions (Hastie et al. 2001).
Model averaging involves the fitting of several plausible models to the data and averaging the results (either parameter estimates or predictions) over all of the
models. The averaging is usually weighted by some
measure of the relative probability or predictive accuracy of each model, with more likely models receiving proportionally more weight (Raftery 1988,
Burnham and Anderson 1998). In this way, poor models receive little weight and have a negligible influence
on the final model. Criteria such as AIC (or variations
thereof) and BIC are often used for this purpose. The
use of BIC in this manner is an approximation to Bayesian model averaging, a process which is technically
complex and computationally demanding, though the
need to use approximations has declined through the
use of increased computational power, and Monte Carlo
simulations can give more accurate results compared
to BIC. As is the case with selection of a single model,
we need some (or at least one) of the models to be a
good approximation to reality for inferences to be unbiased.
The shift from hypothesis testing to estimation, and
use of model averaging to better manage the uncertainty of model selection, does not negate the importance of good sampling design in environmental studies
(Schmitt and Osenberg 1996). Indeed, the additional
uncertainty of model selection is incorporated into the
estimation of effect sizes and thus these estimates will
be less precise, but hopefully more honest, than those
based on a single model.
Attribution of causality
The concept of causality has a long and complex
history and it has many meanings. Its everyday usage
is often straightforward, but as a philosophical or scientific concept, its definition and use are often contentious. At this level, at least three notions of causality
are supported (Pearl 2000, Gillies 2001). First, some
deny the existence of causality or view it as scientifically unnecessary. Second, some acknowledge causality as a useful concept, but do not give it a central role
in their models. Causality is thus seen as a useful way
of explaining some aspects of empirical laws. Third,
some advocate causality as a fundamental construct.
Cause is assumed rather than demonstrated, and in the
formulation of mathematical models, causality takes
Ecological Applications
Vol. 14, No. 5
precedence over probability. Of course, there is no conclusive argument giving universal support to any one
of the three views, and different phenomena can be
used to support differing views, e.g., our everyday experiences support the concept of causality as something
fundamental, but few mathematical models require it.
Statistics is widely accepted within ecology as a primary empirical methodology, yet statisticians are typically not strong advocates of causality as a fundamental construct, favoring probability models instead.
There are statistical approaches that do promote cause
over probability (Pearl 2000), but equally there are
warnings against the causal interpretations (Speed
1990). The randomized experiment is often invoked as
one method for unambiguously determining causality,
but even that is questionable when outcomes are stochastic and we rely on statistical interpretation.
Causal arguments are needed in ecosystem management in order to convince interested parties that management actions should be implemented and will be
effective. These arguments need to balance scientific
rigor with ease of communication to nonscientists. This
situation is not novel and we can borrow from epidemiology, which deals with issues of comparable complexity to the ecological and environmental sciences
and also has similar requirements of scientific rigor and
communication. Epidemiologists developed criteria to
assess causality as part of the research into the link
between cigarette smoking and lung cancer. This link
was accepted by the Surgeon General after decades of
research (U.S. Department of Health, Education, and
Welfare 1964) when evidence compiled from multiple
sources of information and numerous studies fulfilled
a set of criteria (Hill 1965), the main ones being:
1) The relationship between the dose (the putative
cause) and the response should be monotonic.
2) The association between the dose and the response
should be strong.
3) The response should be specific to the cause.
4) There should be a logical time sequence of events;
i.e., the response should occur after the dose has been
applied.
5) There should be consistency both across populations within a study, and with results from other studies.
6) The observations should agree with known biological facts.
These criteria (or subsets, extended sets, or redefined
sets of them) are routinely used in epidemiology to
judge whether or not an association is causal. None of
the criteria are taken as indicative by themselves, but
equally, none are seen as absolutely necessary to evaluate causal significance of associations (Roth et al.
1982). The more criteria that are satisfied and the stronger the association, the more confidence we should
have in our judgment that the association is causal.
Similar criteria have been proposed for ecoepidemiological studies (Fox 1991) and impact assessment stud-
October 2004
1451
FIG. 1. Maps of the northern Great Barrier Reef and the study regions. (a) The risk of exposure to agricultural runoff is
shown in four shades of gray indicating (from dark to light) high, moderate, small, and minimal risk (from Devlin et al.
2002). Boxes surround the two study regions (PC, Princess Charlotte Bay; WT, wet tropics). Also shown are the locations
and names of inshore target reefs (black circles) in (b) PC and (c) WT, and locations of additional reef surveys across the
continental shelf (smaller gray circles), and estuaries of the main rivers affecting the regions.
ies (Schroeter et al. 1993, Stewart-Oaten 1996 b, U.S.

Environmental Protection Agency 1998). The criteria
may need to be adapted or interpreted for particular
studies; e.g., the doseresponse relationship may be
non-monotonic due to toxicity, and the strength of the
relationship could be expressed in many ways dependent on how dose and response are measured. In this
work, we formalize these procedures and extend its use
to multiple possible causes.
We have argued that a shift from the use of hypothesis tests to estimation of parameters, and adoption of
better model selection processes or model averaging
can lead to more informative analyses of the detection
of change. We have also suggested that causal criteria
can be used to rigorously yet transparently attribute
causality. Finally, by selecting combinations of ecological attributes that are complementary with respect
to possible causes of change, we can better discriminate
between likely agents of change, and reduce the likelihood of confounding that may lead to spurious findings. The chosen attributes may be aspects of the physical-chemical environment (either measured directly or
as proxies), abundances and biodiversity of key species
groups, or ecological processes. These processesimproved statistical analysis, use of epidemiological causal criteria, and selection of combinations of complementary ecological attributescan lead to more effective ecological assessments, and we illustrate this in
the following case study.
THE CASE STUDY
Increasing terrestrial runoff of nutrients, sediments
and pesticides is a major management issue facing the
Australian Great Barrier Reef (GBR), but the presence
of measurable effects of runoff on inshore areas has
been controversial (Bell 1991, Larcombe and Woolfe

1999, van Woesik et al. 1999, Haynes and MichalekWagner 2000, Brodie et al. 2001, Devlin et al. 2001,
Furnas 2003, McCulloch et al. 2003). River discharges
are the principal source of nutrients and sediments for
the shallow continental shelf waters (Furnas and Mitchell 2001), and land clearing for agriculture, removal of
soil-retaining wetlands, and intensive use of agricultural chemicals have increased nutrients and sediments
in these discharges three- to 11-fold since European
settlement in 1850 (Furnas 2003). Discharges from the
423 000-km2 catchment area contained 1114 3 106 Mg
of sediment in 2002 compared with 14.4 3 106 Mg
before 1850, and trends of increasing soil erosion are
recorded in coral cores (McCulloch et al. 2003). Further, 100 000 Mg of nitrogen and 20 000 Mg of phosphorus fertilizers are now applied to the catchments
annually, though how much of it eventually enters the
marine system is unknown (Furnas 2003). A region
along the 200 km long wet-tropical coastline between
Tully and Port Douglas containing 60 coral reefs within
20 km from the coast (latitude 188009 to 168209 S,
longitude 1468109 to 1458309 E; Fig. 1) has been identified as the area of greatest risk from agricultural runoff (Devlin et al. 2002). However, causal links between
pollution and reef degradation in this region have been
difficult to demonstrate. This is due to factors such as
a lack of historical data, the large spatial scale, the
presence of natural cross-shelf gradients in community
structure (Dinesen 1983) and suspended particulate
matter (Furnas 2003), and the presence of other types
of disturbance. As in many environmental impact studies, there is no spatial replication for impacted and
nonimpacted regions. Furthermore, the spatial and temporal variability of the flood-related episodic river dis-
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Vol. 14, No. 5
PLATE 1. A naturally turbid but highly diverse inshore reef in Princess Charlotte Bay.
Photo credit: K. Fabricius.
charges of several pollutants is high, and the fate of

pollutants while undergoing dilution, biological uptake, sediment burial, and repeated resuspension during
the transport from river to reef is little understood.
Finally, ecological responses (linear or threshold relationships, synergistic responses) vary greatly across
the multitude of organisms that characterize the highly
diverse coral reef ecosystem.
Around well-defined point sources such as sewage
outfalls or coastal developments, increased sediments
and nutrients are known to cause local reduction in
coral recruitment, increase mortality, and shift the dominance from hard corals to non-reef building organisms
(Smith et al. 1981, Wittenberg and Hunte 1992, Hunter
and Evans 1995). Results from laboratory and field
experiments also demonstrate detrimental effects of
sedimentation and pesticides on individual organism
groups and life stages (Rogers 1990, Dubinsky and
Stambler 1996, Jones et al. 2003, Philipps and Fabricius 2003). While enhanced concentrations of inorganic nutrients appear to have no direct effects on coral
health (Szmant 2002), they can affect coral populations
indirectly, e.g., by shifting competitive advantages toward otherwise nutrient-limited algae when grazing
pressure is low (McCook 1999), or by the formation
of marine snow (Fabricius et al. 2003). Thus, while
causal links between pollution and reef degradation
have been difficult to demonstrate at regional scales
such as the inshore reefs of the GBR, pollution impacts
are well documented and accepted at local scales and
under controlled conditions.
In this study, we assess possible associations between the state of some GBR inshore reefs that are
exposed to terrestrial runoff, but have also been exposed to a number of other disturbances. This case
study has a high political and environmental profile,
both locally due to large economic interests in a healthy
reef through tourism revenues, and globally since landbased pollution and coastal development put 22% and
30%, respectively, of coral reefs on Earth at risk (Bryant et al. 1998).
METHODS
Field data
The study is based on water quality analyses, and
ecological surveys of benthic cover, biodiversity, and
octocoral community structure. Only summaries of the
relevant water quality and ecological surveys are presented here; other laboratory and field studies have
been or will be described in greater detail elsewhere
(Fabricius et al. 2003, Phillips and Fabricius 2003,
Diaz-Pulido and McCook 2003; K. E. Fabricius, G.
Death, E. Turak, and D. Williams, unpublished manuscript).
Study sites and survey methods.The field research
was carried out in two regions within the Great Barrier
Reef (GBR), with one-off surveys characterizing 54
reef sites across the whole continental shelf, and targeted research on 13 inshore reefs (Fig. 1). The wet
tropics (WT) lies between Tully and Port Douglas, and
inshore reefs experience local river plumes from agricultural catchments on an almost annual basis, and
large plumes from the distant Burdekin River on a decadal basis (Furnas 2003). This region has the highest
exposure to runoff from agricultural areas within the
GBR (Fig. 1a; Devlin et al. 2002). The second region
lies north of Princess Charlotte Bay (PC) and ;400
km north of WT, and the inshore reefs are exposed to
runoff from sparsely populated catchments that have
received little or no fertilizer and pesticides to date,
but have low-density cattle grazing in some parts (see
Plate 1). Both regions contain turbid inshore reefs in
similar geophysical settings, located within 20 km of
the coast at 1218 m depth of the surrounding sea floor,
and protected by a barrier of mid- and outer-shelf reefs
up to 40 km offshore (Fig. 1b and 1c). In WT, most
discharged material is eventually transported northward away from the reefs, whereas the large northfacing PC creates anticyclonic eddies which result in
trapped and deposited sediment (Torgersen et al. 1983).
The research on the inshore target reefs was conducted
between 2000 and 2002. An additional 40 mid- and
October 2004
outer-shelf reef sites were visited within the two regions for cross-shelf one-off surveys of benthic cover
and octocoral communities.
The detailed disturbance histories of individual reefs
are largely unknown. In the WT, some reefs experienced outbreaks of the coral-eating crown-of-thorns
seastar Acanthaster planci in the late 1990s, tropical
cyclones in 1986 and 1990, and mortality through coral
bleaching (the expulsion of symbiotic algae from the
coral tissue, primarily caused by high temperatures) in
1998, with bleaching estimated as moderate to extreme on most reefs (Berkelmans and Oliver 1999).
In PC, no data exist for crown-of-thorns seastar (high
numbers were observed on a reef neighboring the inshore target reefs in 1991), but four tropical cyclones
have passed through the region within the last two decades. It is likely that the PC inshore target reefs did
not bleach in 1998 since satellite-based estimates of
sea surface temperatures were near-normal, but some
reefs did suffer severe bleaching mortality in early
2002 after the surveys were completed and during the
coral settlement experiment. The data on crown-ofthorns, cyclone, and bleaching disturbance history
were insufficient to assess or attribute effects on the
scale of individual reefs. In order to distinguish between the potential causes of change, a combination of
ecological attributes with contrasting responses to
bleaching, crown-of-thorns seastar predation, runoff,
and cyclones were chosen for the study. The chosen
attributes were:
1) Benthic cover of hard corals, octocorals, and macroalgae. These are the main groups of organisms usually measured in the assessment of coral reefs, and were
expected to respond to changing environmental conditions and disturbances in contrasting ways.
2) Taxonomic richness of zooxanthellate and azooxanthellate octocorals (Anthozoa, Octocorallia; commonly termed soft corals and sea fans). This
group contains genera with and without symbiotic algae (called zooxanthellae) in their tissue, the former
group depending on water clarity and light for photosynthetic nutrition, whereas the latter group is independent of water clarity (Fabricius and Death 2001).
Octocorals were chosen as indicators for ecological
attributes because of their abundance, and because they
respond more specifically to water quality than hard
corals; azooxanthellate octocorals (which constitute
about half of the genera) do not suffer from coral
bleaching, while zooxanthellate octocorals respond
strongly to turbidity, probably because of low photosynthetic efficiency (Fabricius and Klumpp 1995). Octocorals are also rarely eaten by crown-of-thorns seastar (Death and Moran 1998).
3) Community structure of octocorals on both the
inshore target reefs and along the cross-shelf chlorophyll gradient. This measure was chosen because communities are known to respond more strongly to en-
1453
vironmental conditions than abundances of the main

groups (K. E. Fabricius, unpublished data).
One-off rapid ecological assessment surveys (Fabricius and Death 2001, Fabricius and Alderslade
2001) were used to characterize the ecological condition of 54 reef sites across the continental shelf in both
regions, and 13 inshore target reefs in both regions.
Surveys were conducted on two sites per reef (windward and leeward sides) at five depth zones per site
(018 m); each survey at each depth zone covered
;500 m2 of reef area. Survey data were collected on
percentage cover of the main benthos groups (hard coral, octocoral, macro algae, turf algae, coralline algae,
sand and rubble) and taxonomic inventories and abundance estimates (rating 05) of all genera of octocorals.
Water quality data.Two sets of water quality data
were available from the two regions. First, a 10-yr data
set of chlorophyll concentrations at sites across the
continental shelf on the GBR in both regions (J. Brodie,
G. Death, M. Skuza, and M. Furnas, unpublished manuscript). The chlorophyll measurements were sampled
up to 12 times a year at each site. Second, water quality
data were collected around the inshore target reefs.
Concentrations of water quality parameters (suspended
solids, particulate nitrogen and phosphorus, nitrate, nitrite and ammonium, phosphate, total dissolved nitrogen and total dissolved phosphorus, chlorophyll and
phaeopigments, salinity and silicate) were determined
from water samples taken at each of the inshore target
reefs during nine visits between December 2000 and
April 2002. Water analyses followed standard procedures (Furnas and Mitchell 1996). Only a short section
of the chlorophyll gradient is represented in the inshore
water quality samples, as the innermost reefs in PC
were avoided due to the likely presence of saltwater
crocodiles (Crocodylus porosus). All nutrient data except salinity were highly correlated and they were standardized (z scores) and summed to form a water quality index for each reef. Low index values correspond
to water with low nutrients, chlorophyll, and suspended
particles.
Statistical methods
The analytical methods of this study did not include
the use of hypothesis tests for the reasons argued in
the Introduction. Instead, we estimated effect sizes and
predicted values with interval coverages. Inferences
were based on model averaging, cross-validated
smoothing splines and bootstrap estimation. For each
of these methods, the numerical results can be interpreted from either frequentist or Bayesian perspectives,
but of course the interpretations differ in each case.
All data analyses used S-Plus (Statistical Sciences
1999).
The relationships between chlorophyll concentrations and octocoral richness (zooxanthellate and azooxanthellate) were modeled for each region (WT and
PC) as a function of relative cross-shelf distance (de-
1454
fined as the distance of a site from the coast divided

by sum of distances from the coast and the edge of the
outer continental shelf). The relationships of the responses with relative cross-shelf distance were nonlinear, and smoothing splines were used with the degree
of smoothing estimated by cross-validation (Hastie and
Tibshirani 1990).
The water quality data and chlorophyll data were preanalyzed prior to inclusion in models relating the benthic variables to gradients. To investigate the relationships between the inshore water quality variables, a
principal components analysis was used. A water quality index was then calculated as the sum of all standardized (z scores) variables other than salinity, and
scores on this index were used as measures of water
quality for each reef in subsequent analyses. The ecological survey data and the long-term chlorophyll data
were not recorded at identical sites, hence chlorophyll
levels at the survey sites were estimated by the weighted mean of nearest neighbors from the chlorophyll
sites.
Three sets of ecological attributes, namely (1) benthic cover (hard corals, octocorals, and macroalgae),
(2) taxonomic richness (zooxanthellate and azooxanthellate octocorals), and (3) community composition
(all octocorals) were related to gradients (either chlorophyll or inshore water quality) and regional (WT vs.
PC) differences. For both the chlorophyll and water
quality gradient analyses of benthic cover and richness,
log-linear regression models with linear gradient effects and categorical regional effects were used since
variation increased with the mean and the implicit log
transformation helped linearize gradient effects. For
each response, five models were fitted (1) different
slopes (gradient effects) within each region and different intercepts (region effects), (2) same slope for
both regions, but different intercepts (region and gradient effects), (3) single gradient common to both regions, (4) no gradient effect but region effects, and (5)
no gradient or region effects. The regional effects were
included to account for biological differences due to
region, which were partly confounded with the gradients. The data sets were small with ;50 and 1320
observational units for the chlorophyll or inshore water
quality data respectively.
Preliminary analyses indicated relatively weak associations between the responses and explanatory variables for the smaller data sets, and suggested that conclusions based on hypothesis tests may not adequately
reflect seemingly consistent patterns across the chlorophyll and inshore water quality data. Thus, in order
to select an optimum form of analysis, we conducted
simulations based on estimates of effect sizes and error
obtained from preliminary analyses of benthic cover
and richness gradient data. These simulations showed
BIC (Schwarz 1978) to be marginally better than both
AIC and AICc (Burnham and Anderson 1998) for model selection, and much better than hypothesis tests (see
Vol. 14, No. 5
Appendix). However, none of these methods reliably

selected the true model, and model averaging (Raftery
1988, 1995) gave slightly better predictions than single
best models. Hence, we have used model averaging for
all gradient analyses of benthic cover and richness.
Confidence (credibility) intervals were obtained by
bootstrapping (Efron and Tibshirani 1993, Davison and
Hinkley 1997).
Redundancy analyses (RDA; Rao 1964, Jongman et
al. 1995) were used to assess the dependence of octocoral communities on regional differences (WT and
PC) and on both cross-shelf chlorophyll data and inshore water quality data. The abundances of octocorals
were fourth-root transformed to downweight dominant
taxa, and reef averaged over depths and sites. For community analyses involving the chlorophyll gradient,
relative distance across the shelf was also included.
Ecological gradients were relatively short (moderate
species turnover) thereby justifying the use of RDA,
which requires linear changes of species along gradients. The strengths of regional and gradient effects
were quantified by bootstrapping (Efron and Tibshirani
1993, Davison and Hinkley 1997) the pseudo-F statistic
(ter Braak 1992).
Synthesis
To successfully use the causal criteria, both the ecological attributes and the criteria have to be defined for
each study individually. Our ecological attributes were
cover of hard corals, octocorals, and macroalgae, species richness of zooxanthellate and azooxanthellate octocorals, and community structure, across the shelf
along the chlorophyll gradient and on the inshore target
reefs along the water quality gradient. The criteria were
slightly modified from Hills initial list (Hill 1965) to
best reflect the nature of the case study, using the following definitions:
1) Doseresponse relationship was satisfied if the
probability of gradient effect was .0.99. This corresponds to a Bayes factor of 100:1 and can be taken as
strong evidence for a relationship between dose and
response (Raftery 1995).
2) Strength of association was defined by effect size.
A strong effect was defined as .100% increase (or 50%
decrease) along 80% of the length (to exclude extreme
values) of the inshore water quality gradient within WT.
3) Logical time sequence indicates that the change
did not precede exposure to the disturbance. An assessment of this criterion relies on historic data from
the study regions, which were sparse in our case (no
data exist from the remote PC, and only a few observations exist from WT; Ayling and Ayling 2002; AIMS
Long-Term Monitoring Program, unpublished data).
4) Consistency across populations was defined as
consistency with other studies (i.e., responses recorded in our study were similar to those reported from
other regions in independent published studies).
October 2004
TABLE 1.
(PC).
1455
Comparison of water quality values around inshore reefs of the wet tropics (WT) and Princess Charlotte Bay
PC
WT
Inshore water quality
Mean
SE
Mean
SE
Ratio
Suspended solids (SS; mg/L)

Chlorophyll (Chl; mg/L)
Phaeopigments (phae; mg/L)
Particulate nitrogen (PN; mmol/L)
Nitrate (NO3; mmol/L)
Ammonium (NH4; mmol/L)
Nitrite (NO2; mmol/L)
Total dissolved nitrogen (TDN; mmol/L)
Particulate phosphorus (PP; mmol/L)
Total dissolved phosphorus (TDP; mmol/L)
Silicate (Sil; mmol/L)
Salinity (Sal; g/L)
1.40
0.40
0.19
1.41
0.024
0.16
0.012
8.46
0.096
0.43
4.04
31.8
0.13
0.04
0.03
0.13
0.01
0.02
0.002
0.59
0.012
0.06
1.19
0.48
3.77
0.56
0.32
2.55
0.14
0.24
0.019
8.38
0.16
0.56
9.46
29.1
0.84
0.09
0.06
0.38
0.07
0.08
0.003
1.01
0.03
0.06
2.59
1.54
2.69
1.40
1.68
1.81
5.83
1.50
1.58
0.99
1.67
1.30
2.34
0.93
CI
3.99
1.99
2.73
2.49
27.4
2.67
2.46
1.34
2.55
1.92
6.38
1.01
.0.99
0.93
0.96
0.99
0.88
0.83
0.96
0.49
0.97
0.93
0.99
0.02
95%
1.49,
0.93,
0.97,
1.27,
0.71,
0.55,
0.99,
0.75,
1.01,
0.95,
1.08,
0.82,
Notes: The table lists means and standard errors for each region together with the ratio for WT/PC, 95% confidence
(credibility) intervals based on bootstrap resampling, and the probability that the WT/PC ratio is .1. The intervals can be
treated as confidence intervals or credibility intervals with a non-informative prior.
5) Specificity referred to responses that were known

(from published literature) to be caused by runoff and
was unlikely to be caused by another disturbance type.
6) Agreement with biological facts was scored by
comparing the responses found in our field surveys
with the results of studies where relationships were
directly assessed through manipulative experiments.
By applying each of Hills criteria to each of the
ecological attributes, we created a matrix that was used
to determine to which extent the observed types or
changes in the inshore coral reefs might have been
caused by exposure to runoff. Criteria 13 (doseresponse relationship, strength of association, and logical
time sequence) were assessed based on the relationships between the ecological attributes and the two
water quality data sets. Criteria 46 (consistency with
other studies, specificity of response, and agreement
with biological facts) were scored by comparing the
responses of the ecological attributes with results from
other independent sets of published studies (laboratory
experiments on pollution effects, and data from polluted locations in other regions). For ease of communication, we summarized all results in the matrix by
scoring each cell in one of three possible ways (cells
that could not be addressed due to the lack of data were
marked with na): agreement of the response of the
attribute with the criterion (11), weak or inconclusive response due to inconsistent results or weakness
in the study design (0), responses that are in disagreement with the criterion (21). The overall evidence for a causal association with water quality was
then assessed as the sum over all cells for each of the
ecological attributes, expressed as proportion of the
total number of cells for each attribute for which data
were available.
RESULTS
Field data
Regional differences in water quality and ecological
attributes on inshore target reefs.Mean concentra-
tions of suspended solids, particulate nitrogen, and particulate phosphorus were 170270% higher in the water
around the WT reefs than in the water around PC reefs,
and mean nitrate levels were 580% higher in WT than
in PC (Table 1). Concentrations of other dissolved and
particulate nutrients were also at least as high or higher
in WT than in PC. All water quality variables except
salinity were highly correlated, and most of the inshore
target reefs in WT were exposed to higher nutrient and
sediment concentrations than in PC (Fig. 2).
The ecological attributes of WT also differed substantially from those of PC. On WT reefs 67.7% 6
5.6% (mean 6 1 SE) of space was covered in algae
(turf, coralline, and macroalgae). In contrast, algae occupied 39.6% 6 5.4% of space on PC reefs. Coral cover
was lower in WT than in PC (mean hard coral cover,
15.1% 6 2.4% vs. 43.4% 6 1.0%; octocorals, 2.8% 6
0.8% vs. 5.2% 6 1.5%). The richness of octocorals
was also lower in WT than in PC (25.5 6 2.4 vs. 35.6
6 2.3 genera per reef). In contrast, dead coral cover
in WT was higher than in PC (17.2% 6 6.0% vs. 3.8%
6 0.4%).
Changes in ecological attributes along the chlorophyll gradient across the continental shelf.The gradients in mean water column chlorophyll concentrations across the continental shelf differed between PC
and WT (Fig. 3). In WT, chlorophyll increased steeply
towards the coast, and was up to three times higher in
the innermost 20 km of the region than offshore or in
PC. In PC, chlorophyll remained constant and relatively low across the shelf. Changes in the taxonomic
richness of octocorals across the continental shelf also
showed clear patterns. Richness of zooxanthellate octocorals (genera that contain symbiotic algae in their
tissue and depend on water clarity and light for their
nutrition) declined by 30% in the WT inshore region
within the innermost 20 km of the shelf where chlorophyll was high (Fig. 3). In contrast, no clear crossshelf changes in richness of the zooxanthellate genera
1456
FIG. 2. Principal components biplot of water quality data

(log-transformed and z-score-transformed) at inshore target
reefs in the two study regions (gray, Princess Charlotte Bay;
black, wet tropics). The first two components accounted for
78.6% of water quality variation. Each symbol represents a
target reef, for which data were averaged over within-reef
locations and sampling times; the extent of fill of the symbols
represents octocoral richness, with lowest and highest richness displayed as open and completely filled symbols, respectively. Reefs from the same region are surrounded by a
polygon. Vectors of the water quality variables and water quality index point at reefs with highest concentrations. Abbreviations of the water quality variables are listed in Table 1.
were apparent in PC where chlorophyll was stable

across the shelf. The richness of octocorals without
zooxanthellae (which do not require light for their nutrition) varied little across the continental shelf in WT
and PC and appeared unrelated to the chlorophyll gradient.
Some of the ecological attributes varied systematically along the chlorophyll gradient in both regions
(Fig. 4, Table 2). Macroalgal cover increased with increasing chlorophyll concentrations in both regions.
While hard coral cover was highly variable and unrelated to chlorophyll and region, octocoral cover declined with chlorophyll, reaching lowest cover at a
chlorophyll concentration of .0.3 mg/L. The richness
of zooxanthellate octocorals decreased with increasing
chlorophyll, whereas the richness of azooxanthellate
octocorals was unrelated to chlorophyll.
Octocoral communities showed strong cross-shelf
(pseudo-F 5 9.52), chlorophyll (pseudo-F 5 5.02), and
regional effects (pseudo-F 5 3.13; Fig. 5, Table 3).
Community composition varied most along the chlo-
Vol. 14, No. 5
rophyll gradient within the WT region, with highest

chlorophyll levels associated with lowest richness. Few
genera occurred in areas of high chlorophyll concentrations, and these conditions were only found on some
of the WT inshore reefs. While mid-shelf reefs had
highest richness, some wave-exposed outer-shelf reefs
also had relatively low richness, but were characterized
by a very different suite of species than the low-diversity high-chlorophyll near-shore reefs.
Changes in ecological attributes along the water
quality gradients on the inshore target reefs.Changes
in ecological attributes along the inshore water quality
gradient were weaker than those along the chlorophyll
gradient across the shelf, most likely because of the
relative shortness of the inshore gradient and the lower
number of inshore reefs (1320). Nonetheless, three of
the ecological attributes varied along the water quality
gradient in similar ways to the cross-shelf variation
along the chlorophyll gradient (Fig. 4, Table 2). Only
one of the three effects would have been detected had
frequentist tests been used for the analyses (Table 2).
Macroalgal cover increased along the water quality gradient in WT around threefold, but was variable in PC.
Hard coral cover and the richness of azooxanthellate
octocorals both showed strong regional differences, but
were unrelated to the water quality gradient. Octocoral
cover was similar in both regions and also appeared
unrelated to water quality. In contrast, the richness of
zooxanthellate octocorals declined with increasing nutrients along the water quality gradient in both regions.
The octocoral communities varied most strongly
along the water quality gradient (pseudo-F 5 3.39,
Table 3) and to a lesser degree between regions (1.25).
Generic richness was highest in clear water PC reefs,
and most genera were absent or occurred in low numbers in WT water of low water quality (Fig. 6). Within
each region, reefs associated with the highest nutrient
and sediment levels were those with lowest richness
and vice versa. Only two octocorals species (the encrusting Briareum sp. and Clavularia koellikeri) were
associated with high nutrients, whereas a large proportion of genera were strongly associated with the
low-nutrient PC reefs.
Synthesis
We combined the results of our field study with results from other regions and from laboratory experiments, and used Hills causality criteria to evaluate the
potential link between water quality and the condition
of the inshore coral reefs. The results were expressed
concisely in matrix format with the rows of the matrix
(Table 4) defined by the criteria, and the columns by
the ecological attributes, namely, cover of the main
benthos groups, richness of zooxanthellate and azooxanthellate octocorals, and community structure.
Doseresponse relationship.There was strong evidence for doseresponse relationships for three of the
five ecological attributes both along the cross-shelf
October 2004
1457
FIG. 3. Cross-shelf gradients in mean chlorophyll concentrations, based on 10 years of chlorophyll monitoring data and
taxonomic richness in octocorals with and without zooxanthellae (PC, Princess Charlotte Bay; WT, wet tropics). Thick solid
lines indicate cross-validated smoothing splines; thinner lines are 95% confidence intervals. Vertical light gray bands indicate
the locations of the inshore target reefs across the shelf.
chlorophyll gradient and along the water quality gradient on the inshore target reefs (Fig. 4, Tables 2 and
3). Doseresponse relationships were established for
macroalgal cover, octocoral cover, generic richness of
zooxanthellate octocorals, and octocoral community
structure. In contrast, hard coral cover, although much
lower in WT than in PC, was unrelated to the chlorophyll and inshore water quality gradients, possibly
due to the effect of other disturbances. The richness of
azooxanthellate octocorals was also unrelated to water
quality, as expected from their biological requirements.
In all of the relationships, the directions of change (i.e.,
increase or decrease along the water quality gradient,
or differences between regions) agreed with those expected from existing biological knowledge.
Strength of association.Some of the effects along
the water quality gradient across the shelf and within
the WT inshore region were large and ecologically significant (Fig. 4, Table 2). Macroalgal cover was 3.1
times higher on the reefs with highest nutrient and particle loads compared with those in clearest water in
WT. The number of octocoral genera was 2.4 times
higher on WT reefs with clearest water compared with
those in the least clear water. Associations between
community structure and the water quality and chlorophyll gradients were stronger than the differences
between the regions (Table 3), with depauperate communities recorded in the reefs with highest nutrient and
particle loads.
Logical time sequence.The assessment of this criterion is limited by the scarcity of historic data. Few
data exist to compare the ecological attributes on any
of the inshore target reefs with those from the past, and
some differences between the two regions in biodiversity are likely to have always existed due to the natural
decline in biodiversity with increasing latitudes. The
only historic data available are for one reef in the WT
region where hard coral cover decreased from ;80%
in 1989 to the present state due to a number of disturbances (Ayling and Ayling 2002). The logical time
sequence criterion of water quality effects on coral
reefs has however been met in other places, e.g., in
Hawaii, where coral cover increased and algal cover
decreased following offshore diversion of a coastal
sewage outfall site (Smith et al. 1981, Hunter and Evans
1995).
Consistency across different studies.The findings
of increased macroalgal cover and low hard coral cover
are consistent with previous work in other coral reef
regions exposed to terrestrial runoff (e.g., Tomascik et
al. 1993, Edinger et al. 2000, Hodgson and Yau 1997,
van Woesik et al. 1999, West and Van Woesik 2001).
Few studies have included octocorals, but species richness in response to disturbance have been reported for
other groups of reef organisms (Edinger et al. 1998).
The response of zooxanthellate octocorals, and the absence of a response in azooxanthellate octocorals are
consistent with a study on larger scale on the relation-
1458
Vol. 14, No. 5
FIG. 4. Relationship between ecological reef attributes and chlorophyll and water quality. Gray and black lines and circles
indicate reefs within the PC and WT regions, respectively. Solid lines indicate the model-averaged predictions from loglinear model fits, dashed lines indicate 95% confidence (credibility) intervals derived by bootsrapping, and the (pseudo-) R2
are the explained deviance of the model-averaged fit divided by the deviance of the null model. The left column of plots
shows variation of ecological attributes along the chlorophyll gradient across the continental shelf, and the right column
similarly for the water quality index, calculated as the sum of the z scores of all water quality variables excepting salinity
of each reef at inshore target reefs (high index values, high nutrient concentrations; low values, cleaner water). Ecological
attributes are: HC, hard corals; OC, octocorals; MA, macroalgae; zoox, zooxanthellate; azoox, azooxanthellate. Richness is
defined as the number of genera of octocorals per reef encountered during swim surveys.
October 2004
1459
TABLE 2. Analyses of models relating ecological responses to (a) chlorophyll gradients and cross-shelf regions and (b)
inshore water quality gradients and regions.
R1G
)
exp(G
a) Cross-shelf (chlorophyll)
MA cover (%)
0.03
HC cover (%)
0.00
OC cover (%)
0.19
OC richness (zoox)
0.10
OC richness (azoox)
0.07
0.17
0.02
0.44
0.15
0.40
0.80*
0.10
0.37*
0.75*
0.00
0.00
0.14
0.00
0.00
0.52*
0.00
0.73*
0.00
0.00
0.01
0.91
20.01
21.49
20.75
0.29
2.48
0.99
0.23
0.47
1.34
b) Inshore (water quality index)

MA cover (%)
0.39
HC cover (%)
0.11
OC cover (%)
0.24
OC richness (zoox)
0.05
OC richness (azoox)
0.09
0.21
0.27
0.28
0.19
0.29
0.24
0.00
0.21
0.72*
0.26
0.06
0.62*
0.25*
0.02
0.36*
0.10*
0.00
0.02
0.01
0.00
1.12
0.03
20.01
20.34
20.24
3.06
1.03
0.99
0.71
0.79
Variable
R3G
CI
1.93,
0.92,
0.15,
0.38,
0.95,
3.18
1.07
0.34
0.60
1.95
.0.99
0.61
.0.99
.0.99
0.04
1.61,
0.82,
0.60,
0.59,
0.55,
6.71
1.32
1.61
0.87
1.13
.0.99
0.39
0.51
.0.99
0.91
95%
Notes: Abbreviations: MA, macroalgae; HC, hard coral; OC, octocoral; zoox, zooxanthellate; azoox, azooxanthellate. Loglinear models were used for all analyses. In the models, the gradient (G) effects are linear, and the region (R) effects are
categorical. For each ecological response, five models are compared: R 3 G, different gradient effects (slopes) within each
region and different region effects (intercepts); R 1 G, same slope but different region effects; G, single slope common to
both regions; R, no gradient effect but regional effects; and 1, no gradient or regional effects. The best model (most likely
according to Bayes information criteria [BIC]) is denoted by boldface text, and the best model selected by backward elimination
of nonsignificant terms (P . 0.05) is indicated by an asterisk. For four of the 10 models, the most likely model was not
selected by backward elimination. For four of the models, the relative probability for the most likely model is low (,0.5).
), proportional change (exp(G
)),
Models were averaged, weighted by the relative probabilities, and the estimated gradient (G
and 95% confidence (credibility) interval (CI) were estimated. For macroalgal cover (expected to increase along the gradient),
the probability (P) that proportional change was .1 is shown; for other responses, the probabilities of decline are shown.
For each response, the predicted values weighted by the relative probabilities and averaged across models are shown in Fig. 3.
ship between octocoral richness and water clarity (Fabricius and Death 2001).
The response is specific for the cause, thus an association should be stronger if there are few rather
than many causal factors.Some, but not all of the
responses were specific to water quality. In particular,
total hard coral cover is a nonspecific response, as it
may be low after a bleaching or crown-of-thorns disturbance, or it may be high even in chronically adverse
conditions due to the asexual spread of a few resistant
species. Macroalgal growth increases with nutrients,
and unlike corals is not known to be affected by periods
of high temperatures. Macroalgal cover remains low
despite high nutrient levels at high grazing pressure
(McCook 1999), however macroalgal cover is rarely
high in low-nutrient environments, and macroalgae
have established dominance on reefs in some areas of
FIG. 5. Redundancy analysis biplot of octocoral coral communities, showing the dependence on chlorophyll, relative distance across
the continental shelf (across) and region
(gray, Princess Charlotte Bay; black, wet tropics). The first two components shown in the
biplot accounted for 78.6% of the explained variation in octocoral abundances. Each symbol
represents a reef, and the fill of the symbol represents the generic richness in octocorals of that
reef. Chlorophyll and distance of the reefs
across the shelf are represented as vectors and
point in the directions of highest chlorophyll
loads and offshore reefs, respectively.
eutrophication (Smith et al. 1981). Octocoral cover is

more specific than hard coral cover, as octocorals are
rarely eaten by the crown-of-thorns seastar (Death and
Moran 1998), or indeed any other major group of predators, and azooxanthellate octocorals are unaffected by
coral bleaching. A few octocorals of the families Alcyoniidae, Clavulariidae, and Briareidae may increase
in cover in areas of high nutrient loads, if other physical
environmental conditions such as currents and light are
favorable. However, bleaching-susceptible zooxanthellate genera tend to be more abundant than azooxanthellate genera, and thus octocoral cover may be reduced by bleaching. The decrease in octocoral richness
appears to be specific to water quality. This conclusion
is supported by the rarity of species with low tolerance
of poor water quality, the abundance of some more
tolerant taxa (e.g., Briareum sp.) and the lack of re-
Vol. 14, No. 5
1460
TABLE 3. ANOVA of community composition of octocoral genera showing the effects of (a)
relative distance across the shelf, the chlorophyll cross-shelf gradient and regions (WT and
PC), and (b) the inshore water quality gradient and regions.
Effect
df
SS
a) Cross-shelf
Across
Chlorophyll
Region
Residuals
1
1
1
51
53.3
28.1
17.5
285.5
b) Inshore
Water quality index
Region
Residuals
1
1
10
16.969
6.285
50.048
MS
SS
(%)
Pseudo-F
95%
CI
53.3
28.1
17.5
5.6
13.9
7.3
4.5
74.3
9.52
5.02
3.13
6.77, 12.82
3.47, 7.44
1.24, 4.92
.0.99
.0.99
0.99
16.9
6.3
5.0
23.1
8.6
68.3
3.39
1.25
1.32, 6.66
0.45, 5.56
.0.99
0.61
Notes: For panel (a) 66 genera were analyzed, and for panel (b) 57 genera were analyzed;
the sequential sums of squares were summed over the responses to give ANOVA tables. The
pseudo-F statistic was bootstrapped and bias-adjusted to give 95% intervals. P denotes the
probability that the true value of pseudo-F was .1 (the expected value of pseudo-F, given
that a variable has no effect). For (a) there were strong effects of relative distance across the
shelf and chlorophyll, and weaker regional differences. For (b) there was a strong effect of
water quality and no effect of region. Reversing the order of inclusion of chlorophyll and
region, and water quality and region, slightly increased the strength of the region effects (;30%)
and correspondingly reduced the chlorophyll and water gradient effects.
sponse in azooxanthellate taxa in WT. Similarly, the

gradients in octocoral community structure, with communities being progressively depauperate with increasing nutrients and sediments, could not be explained by
other major disturbances (cyclones, bleaching, and
crown-of-thorns).
Association agrees with known biological facts.
Increased supply of limiting nutrients is known to increase macroalgal growth rates in the absence of other
limiting factors (Schaffelke and Klumpp 1998). Sedimentation affects recruitment and increases adult mortality in hard and octocorals, thus potentially reducing
coral cover (Riegl and Branch 1995, Fabricius et al.
2003, Philipps and Fabricius 2003). A reduction in biodiversity is likely due to variable tolerances of species
to sedimentation, turbidity, and bleaching. Octocoral
richness is known to decline by one genus per meter
reduction in visibility on the Great Barrier Reef in areas
where visibility is ,10 m (Fabricius and Death 2001),
a finding that matches the decline in richness along the
water quality and chlorophyll gradients in this study.
DISCUSSION
Identifying anthropogenic causes of ecological
change and distinguishing such change from natural
dynamics is a nontrivial task. However causal attribution profoundly enhances the ability of scientists to
contribute to environmental management, and increases the effectiveness of management action. For example, in coral reef ecology the cause(s) of outbreaks
of the crown-of-thorns seastar Acanthaster planci are
still being debated by scientists 40 years after the first
observations of outbreaks. Costly local eradication programs are now in place to protect some tourism sites;
funding that might have been spent on preventative
measures if causes had been identified with a reasonable level of certainty. A contrasting example is that
high sea surface temperatures are now accepted by
most scientists as the major cause of coral bleaching
(Strong et al. 1997), and agreement on the cause of
predicted massive ecosystem changes by coral bleaching is adding momentum to the call for political action
FIG. 6. Redundancy analysis biplot of octocoral coral communities at the inshore target reefs in PC (gray symbols) and
WT (black symbols). The first two components shown in the biplot accounted for all of the explained variation in octocoral
abundances. Each symbol represents a reef, and the fill of the symbol represents the generic richness of octocorals at that
reef. The water quality index vector points in the direction of highest nutrient loads.
October 2004
1461
TABLE 4. Synthesis matrix defined by causality criteria and ecological attributes, summarizing
ecological evidence of terrestrial runoff effects on reefs within the wet tropical region of the
Great Barrier Reef (Fig. 1).
Benthic cover
Richness
Communities
OC Z OC A
OC C OC I
Criteria
HC
OC
MA
A1) Biological gradient: cross-shelf

B1) Effect size: cross-shelf
A2) Biological gradient: inshore
B2) Effect size: inshore
C) Logical time sequence
D) Consistency with other studies
E) Specificity of response
F) Agreement with biological facts
Score
2
2
2
2
1
0
2
1
23/8
1
1
2
2
1
1
1
1
1
1
1
1
2
2
2
0
1
1
1
1
1
1
1
1
NA
NA
NA
NA
NA
NA
NA
NA
NA
NA
1
0
1
2/7
1
1
1
7/7
1
1
1
7/7
1
1
1
0/8
1
5/5
1
5/5
Notes: Data from this region are compared with those from reefs at low risk from runoff in
the Princess Charlotte Bay. Criteria A and B address responses observed in this study (Figs.
46, Tables 23). Criteria CF address the agreement between responses in this study and
results from other runoff-exposed regions and from laboratory studies on pollution effects.
Symbols in the matrix indicate the following: agreement with the criterion (1), inconclusive
(0, inconsistent or weak), disagreement (2), and not addressed due to the lack of data (NA).
Abbreviations: HC, hard coral; OC, octocorals; Z, zooxanthellate; A, azooxanthellate; C, crossshelf; I, inshore. The final row is the sum of scores as the proportion of all scores for each
attribute, scoring 1 as 11, 2 as 21, and ignoring NA.
to combat greenhouse gas emission. While enormous

international commitments are required to halt or reverse global climate change, in our case study the reduction of soil and fertilizer loss through terrestrial
runoff is achievable through integrated river basin management and long-term government support on regional
scales (Brodie 2003).
The use of a framework based on the estimation of
effect sizes to determine change, an established set of
criteria to attribute causality, and a rigorous choice of
ecological attributes with contrasting environmental responses, represents a shift in philosophy and practice
from some of the existing ecological techniques. For
simple ecological analyses, methodologies such as control-impact studies and ecological indicators can effectively detect change, and meta-analysis of multiple
studies can help relate change to potential causes on a
broader scale (Schmitt and Osenberg 1996). However,
for large or complex ecosystems, existing methods are
often insufficient to detect change and attribute causality (Stewart-Oaten 1996a, b). Many forms of evidence of varying strengths are to be considered, e.g.,
field studies with notoriously imperfect controls and
laboratory experiments that oversimplify natural systems. It is therefore not surprising that simple hypothesis tests are unable to resolve such complex questions.
After all, it took decades of extensive and expensive
research for epidemiologists to assemble sufficient evidence to identify cigarette smoking as a cause of lung
cancera link that is obvious in hindsight. Hills method of causal attribution has been recommended by the
Environmental Protection Agency of the United States
(U.S. Environmental Protection Agency 1998), but applications, both on single-factor single-cause analyses,
or on ecosystem analyses, have so far rarely been attempted in the ecological literature.
In our study, we found the inshore reefs in the WT

region to be in a disturbed state. The use of Hills causal
criteria helped us to synthesize and assess a body of
data that quantified the ecological attributes and the
environmental conditions in the two regions, and along
water quality gradients within the regions. The two
biological gradients, the large effect sizes, the consistency across populations and with other studies, and
the agreement with biological facts, all contributed to
enhancing the belief that water quality had an adverse
effect on aspects of the ecological state of these reefs.
These data indicated the existence of causal links between high nutrient loads and high macroalgal cover
as well as low octocoral biodiversity. Hard coral cover
also differed more than two-fold between the two regions. Since the two regions contrasted not only in
water quality but also in exposure to other disturbances
(coral bleaching and coral predation by crown-ofthorns seastar), these strong regional differences could
not be attributed exclusively to water quality, although
responses to these multiple disturbances including water quality may have been cumulative or synergistic.
We found the matrix to be helpful in synthesizing the
data, attributing causality to some attributes while excluding others, and communicating the results to other
scientists and the public.
The scientific understanding of coastal marine systems in the tropics is far less developed than in temperate systems such as Chesapeake Bay or the North
and Baltic Seas, where considerable effort has been
invested into understanding the effects of nutrient enrichment and toxic chemicals. In our case study, the
available data are comparatively sparse. Due to the high
biological diversity of the Great Barrier Reef, we focused on responses of relatively broad ecological
groups rather than of individual key species. It became
1462
apparent that community structure responded more sensitively to water quality than summary parameters such
as benthic cover, indicating that substantial information
is contained in the responses of individual species that
will require follow-up laboratory exposure-effects experiments. It also became apparent that there was little
species replacement in octocorals from clean to turbid
water, rather species increasingly dropped out towards
high nutrient conditions, and only two species appeared
to grow well in the waters with the least clean water.
Although octocorals do not contribute to the formation
of coral reefs, they are the second-most abundant group
of macrobenthos in coral reefs. The disappearance of
a large number of octocoral genera in areas of high
loads of nutrients and suspended particles may be taken
as an indicator for severe deterioration of environmental conditions, with potential consequences for other
organism groups that were not included in the study.
What remained unresolved in our study is the origin
of the high nutrient levels in the water around the inshore target reefs, and thus the direct link between
terrestrial runoff and nutrient enrichment. It may be
argued that nutrient, chlorophyll, and sediment levels
in the marine inshore region of the WT may have always been high. Rivers discharging from catchments
with heavily fertilized sugar crops into the wet tropical
marine system carry levels of nutrients, sediments and
pesticides that are several times higher than estimated
levels in pre-European times and than rivers discharging into Princess Charlotte Bay (Furnas 2003). The
relatively high levels of nitrate measured around the
WT reefs (Table 1) indicate fresh supply of this nutrient, as concentrations of dissolved inorganic nitrogen
are rapidly taken up by nutrient-limited algae and bacteria in tropical marine systems. This supply is likely
to have come from the rivers, which are the largest
source of new nutrients in the GBR lagoon away from
upwelling areas (Furnas et al. 1997, Mitchell et al.
2001). Combined with flood-plume dispersal models
(Devlin et al. 2002), the limited existing data therefore
suggest that modern agrochemicals do reach the target
inshore reefs of the WT where they may contribute to
the measurably higher concentrations of water nutrients. Similarly, it may be argued that coral cover and
biodiversity on the WT reefs may have always been
low. However, the widths of the reef flats around the
islands in both regions indicate positive reef accretion
over extended periods in earlier times (Hopley et al.
1983). Observations on one WT reef group (the Russell-Normanby Islands) show declining coral cover
since 1990 due to a series of disturbances by bleaching,
cyclones, and a crown-of thorns seastar outbreak (Ayling and Ayling 2002), and it appears that the reefs have
failed to recover from these disturbances. Coral cover
has also been monotonously declining on a number of
other WT inshore reefs since 1985 to ;10% cover in
2002 (AIMS Long-Term Monitoring Program, unpublished data). Coral cover can increase by 10% per year
Vol. 14, No. 5
on some inshore reefs after disturbance (Ayling and

Ayling 2002), and anecdotal reports indicated that coral
cover on the Russell-Normanby Islands did recover after tropical cyclones in 1975 and 1977, and reached
pre-cyclone levels in 1990 after a severe tropical cyclone in 1986 (Devantier 1994). This suggests that multiple disturbances have reduced coral cover on WT
reefs, while exposure to terrestrial runoff appears to
retarding coral recovery after the recent disturbances.
In the absence of new disturbances, coral cover may
recover within one to two decades despite continuing
exposure to high levels of nutrients and sediments
(probably through the re-establishment of fast-growing
Montipora and Acropora), whereas the processes and
time frames leading to restoration of coral richness and
presence of more sensitive or slower-growing species
are unknown. Importantly, although changes between
past and present conditions both in water quality and
in the ecological properties of the WT inshore reefs
can not be established with certainty, the ecological
gradients along the water quality gradient (as demonstrated in this study) can serve to predict future changes
in macroalgal cover and octocoral biodiversity, should
the water quality deteriorate or improve as land use
practices change.
To conclude, using the matrix in combination with
modern statistical analyses, we have aimed at overcoming the problems that often prevent the early detection of ecological change and its causes. We have
synthesized multiple and complex sources of information to avoid any misleading selective use of scientific data, and used modern statistical methods to
overcome abuse of technical concepts such as probability and causality. As ecologists, we need to synthesize multiple and complex sources of information,
weigh the evidence, quantify effect sizes, and predict
the ecological consequences and socioeconomic costs
of alternative actions. The matrix framework can help
doing all this. By applying stringent, scientifically robust, yet simple criteria to well-chosen properties of
the ecosystem, we can greatly improve our capacity to
determine change and attribute causality. This should
lead to higher performance benchmarks for complex
ecological studies, and a greater scientific contribution
to sustainable ecosystem management. It is then up to
a better-informed society to decide how much ecological change is acceptable.
ACKNOWLEDGMENTS
We gratefully acknowledge the contributions of Jon Brodie
for providing the long-term chlorophyll monitoring data of
the Great Barrier Reef Marine Park Authority, and of Michelle
Skuza, Jane WuWon, and Margaret Wright for analyzing the
water quality samples. We thank the Subject Editor Paul Dayton, Simon Thrush, and an anonymous reviewer for very helpful reviews and comments. Thanks also to Miles Furnas, Jon
Brodie, David Williams, Britta Schaffelke, Lyndon Devantier,
Janice Lough, and Malcom McCulloch for comments on earlier versions of the manuscript. A number of volunteers and
the crews of the AIMS Research Vessels were a great help
October 2004
in the field studies. The research was funded by the Cooperative Research Centre for the Great Barrier Reef World
Heritage Area (CRC Reef), and the Australian Institute of
Marine Science (AIMS).
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APPENDIX
A table showing simulation results to determine analysis methods for small data sets is available in ESAs Electronic Data
Archive: Ecological Archives A014-031-A1.

Identifying Ecological Change and Its Causes: A Case Study On Coral Reefs

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Ecological Applications, 14(5), 2004, pp.

IDENTIFYING ECOLOGICAL CHANGE AND ITS CAUSES:

Abstract. The successful management of ecosystems depends on early detection of

IDENTIFYING ECOLOGICAL CHANGE AND CAUSE

Statistical issues in the detection of change

with confidence [credibility] intervals (Stewart-Oaten

KATHARINA E. FABRICIUS AND GLENN DEATH

el selection and can be treated as relative probabilities

IDENTIFYING ECOLOGICAL CHANGE AND CAUSE

ies (Schroeter et al. 1993, Stewart-Oaten 1996 b, U.S.

been controversial (Bell 1991, Larcombe and Woolfe

KATHARINA E. FABRICIUS AND GLENN DEATH

charges of several pollutants is high, and the fate of

IDENTIFYING ECOLOGICAL CHANGE AND CAUSE

vironmental conditions than abundances of the main

KATHARINA E. FABRICIUS AND GLENN DEATH

fined as the distance of a site from the coast divided

Appendix). However, none of these methods reliably

IDENTIFYING ECOLOGICAL CHANGE AND CAUSE

Inshore water quality

Suspended solids (SS; mg/L)

5) Specificity referred to responses that were known

KATHARINA E. FABRICIUS AND GLENN DEATH

FIG. 2. Principal components biplot of water quality data

were apparent in PC where chlorophyll was stable

rophyll gradient within the WT region, with highest

IDENTIFYING ECOLOGICAL CHANGE AND CAUSE

KATHARINA E. FABRICIUS AND GLENN DEATH

IDENTIFYING ECOLOGICAL CHANGE AND CAUSE

b) Inshore (water quality index)

eutrophication (Smith et al. 1981). Octocoral cover is

KATHARINA E. FABRICIUS AND GLENN DEATH

sponse in azooxanthellate taxa in WT. Similarly, the

IDENTIFYING ECOLOGICAL CHANGE AND CAUSE

A1) Biological gradient: cross-shelf

to combat greenhouse gas emission. While enormous

In our study, we found the inshore reefs in the WT

KATHARINA E. FABRICIUS AND GLENN DEATH

on some inshore reefs after disturbance (Ayling and

IDENTIFYING ECOLOGICAL CHANGE AND CAUSE

Devlin, M., J. Brodie, J. Waterhouse, A. Mitchell, D. Audas,

KATHARINA E. FABRICIUS AND GLENN DEATH

graphic processes of coral reefs: physical and biological

Newman, M. C., and D. A. Evans. 2002. Enhancing belief

IDENTIFYING ECOLOGICAL CHANGE AND CAUSE

U.S. Department of Health, Education, and Welfare. 1964.

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