Environment International 55 (2013) 71–91

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Environment International
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Review

Assessing and managing sediment contamination in transitional waters

Peter M. Chapman a,⁎, Feiyue Wang b, c, Sandra Sofia Caeiro d, e
a
Golder Associates Ltd., 500-4260 Still Creek Drive, Burnaby, BC V5C 6C6, Canada
b
Center for Earth Observation Science, Department of Environment and Geography, University of Manitoba, Winnipeg, MB R3T 2N2, Canada
c
Department of Chemistry, University of Manitoba, Winnipeg, MB R3T 2N2, Canada
d
Departamento de Ciências e Tecnologia, Universidade Aberta, Rua da Escola Politécnica, 141, 1269-001 Lisbon, Portugal
e
Center for Environmental and Sustainability Research, Departamento de Ciências e Engenharia do Ambiente, Faculdade de Ciencias e Tecnologia, Universidade Nova de Lisboa,
Campus da Caparica, 2829-516 Caparica, Portugal

a r t i c l e i n f o a b s t r a c t

Article history: Sediment contamination remains a global problem, particularly in transitional waters such as estuaries and
Received 9 October 2012 coastal lagoons, which are the recipients of chemicals from multiple near- and far-field sources. Although tran-
Accepted 18 February 2013 sitional waters are highly productive ecosystems, approaches for assessing and managing their sediment con-
Available online 22 March 2013
tamination are not as well developed as in marine and fresh waters. Further, although transitional waters
remain defined by their variable and unique natural water quality characteristics, particularly salinity, the
Keywords:
Estuaries
biota inhabiting such ecosystems, once thought to be defined by Remane's “paradox of brackish water”, are
Lagoons being redefined. The purpose of the present paper is to build on an earlier but now dated (>12 years old)
Contaminants review of methods to assess sediment contamination in estuaries, extending this to all transitional waters, in-
Toxicity cluding information on integrative assessments and on management decision-making. The following are specif-
Bioindicators ically discussed: chemical assessments; bioindicators; biomarkers; and, biological surveys. Assessment and
Biomarkers management of sediment contamination in transitional waters need to be focused on ecosystem services and,
where appropriate and possible, be proactive rather than reactive when uncertainty has been suitably reduced.
© 2013 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 72
2. Transitional waters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 72
2.1. What are transitional waters? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 72
2.1.1. Summary. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73
2.2. Ecology of transitional waters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73
2.2.1. Summary. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73
3. Assessment techniques: chemistry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73
3.1. Unique processes and dynamics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73
3.2. Role of suspended particles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 74
3.3. Role of salinity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 74
3.4. Non-conservative mixing of contaminants in transitional waters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 75
3.5. Cautions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 75
3.6. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 75
4. Assessment techniques: bioindicators . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 75
4.1. Toxicity tests . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 76
4.1.1. Summary. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 77
4.2. Biological surveys . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 77
4.2.1. Summary. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 79
5. Assessment techniques: biomarkers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 79
5.1. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 86
6. Integrative assessments. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 86
6.1. Different approaches to integration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 86
6.2. Dealing with uncertainty . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 86

⁎ Corresponding author. Tel.: +1 604 230 7395.

E-mail addresses: pmchapman@golder.com (P.M. Chapman), Feiyue.Wang@ad.umanitoba.ca (F. Wang), scaeiro@uab.pt (S.S. Caeiro).

0160-4120/$ – see front matter © 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.envint.2013.02.009
72 P.M. Chapman et al. / Environment International 55 (2013) 71–91

6.3. Establishing causation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 87

6.4. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 87
7. Management and decision-making . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 87
7.1. Ecosystem services . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 87
7.2. Management of ecosystem services in transitional water bodies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 87
7.3. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 88
8. Concluding remarks. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 88
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 88
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 88

1. Introduction concludes by suggesting the way forward for both assessment and
management of contaminated sediments in transitional waters.
“Everything is both simpler than we can imagine and more entangled
2. Transitional waters
than we can conceive”.
[Johann Wolfgang von Goethe (1749–1832)]
2.1. What are transitional waters?

Some 12 years ago two of the authors of this paper reviewed
methods for assessing sediment contamination in estuaries (Chapman
and Wang, 2001). Despite being well cited, that review is now dated,
did not include all transitional waters (defined as distinct water bodies
that are partly saline but influenced by freshwater flows), and did not in-
clude biomarkers, integrative assessments, or management options fol-
lowing assessment. Unfortunately, one conclusion from that review
remains valid: most sediment assessment methods are primarily appli-
cable to fresh or salt waters, not to transitional waters.
Also still true today, sediment contamination continues to be an
issue of increasing global importance. And transitional waters continue
to be highly productive ecosystems that provide a wide range of ecosys-
tem services that human communities rely upon (e.g.: preferential
areas for urban and industrial settlement; transportation corridors; rec-
reational facilities for boating; fishing; aquaculture; agriculture), but
which are threatened by sediment contamination from direct and indi-
rect sources (Sun et al., 2012). Because transitional waters are critical to
the life history and development (e.g., rearing, feeding, migration
routes, and nursery grounds) of many aquatic species, sediment con-
tamination in those waters needs to be fully assessed and appropriately
managed.
Chapman and Wang (2001) defined an estuary as “a semi-
enclosed and tidal coastal body of water which has a free connection
with the open sea and within which sea water is measurably diluted
with fresh water derived from land drainage.” Estuaries can be fjords,
river mouths, or tidal creeks. In contrast to estuaries, coastal lagoons
(sometimes classified as secondary estuaries; Perillo, 1995) have a re-
duced freshwater inflow compared to their marine water inflow and
are naturally ephemeral. Lagoon entrances can become restricted or
closed due to storm events pushing sand in from the sea, ultimately
resulting in short-lived lakes. Conversely, if a lagoon entrance be-
comes too large, the lagoon will become a marine bay. Estuaries can
be similarly ephemeral (e.g., from the build-up of deltas), but over
much longer time periods than coastal lagoons.
Many studies and researchers still do not appear to properly ap-
preciate the unique and dynamic nature of transitional waters. The
purpose of this paper is to enhance that appreciation as part of an
updated review of the state-of-the-art of transitional waters sedi-
ment contamination assessment and management methods. The
paper begins with a brief review of transitional waters. It then pro-
ceeds to discuss the following assessment techniques which cannot
be applied in the same manner to those waters as to fully fresh or
marine waters: chemical analyses; bioindicators (i.e., toxicity tests,
biological surveys); and, biomarkers. Other assessment techniques,
which can be applied similarly in transitional and other waters, are
listed in Chapman and Hollert (2006). A discussion on integrative as-
sessments, management and decision-making follows. The paper
Transitional waters are neither wholly fresh (i.e., salinity ~ 0) nor
wholly saline (i.e., salinity > 30); their salinities are generally interme-
diate although variable such that at times they can approximate fresh or
saline conditions. They comprise an interface, but one that occurs in
unique water bodies (e.g., estuaries, coastal lagoons, fjords, rias). Tran-
sitional waters were defined by the European Communities (2000) as
“bodies of surface water in the vicinity of river mouths which are par-
tially saline in character as a result of their proximity to coastal waters
but which are substantially influenced by freshwater flows”. We have
modified this definition to “distinct water bodies that are partly saline
but influenced by freshwater flows” to avoid some of the difficulties in
the original definition as noted by McLusky and Elliott (2007). Our def-
inition encompasses both large and small geographic areas; for in-
stance, the Arctic Ocean which receives massive and increasing inputs
of freshwater from runoff can be considered a transitional water body
(McClelland et al., 2012).
Transitional waters can be vertically stratified (e.g., salt wedge es-
tuaries in river mouths where river flow dominates and saltwater
moves upstream as a “wedge” under the downstream fresh water
flow; shallow estuaries, fjords and coastal lagoons where river flow
is less dominant and is modified by tidal currents). They can also be
vertically homogeneous either consistently or at different time pe-
riods depending on the relative influence of freshwater inputs and
tidal currents. Transitional water bodies can vary seasonally as fresh-
water flow increases or decreases. They include temporarily open/
closed estuaries, which comprise most of the estuaries in South Africa
(Scharler, 2012). The presence of a sill (a ridge at the entrance to a
transitional body of water) can result in oxygen deficiency (hypoxia).
Inverse estuaries occur in arid or semi-arid climates where evapora-
tion greatly exceeds the inflow of fresh water; salinity is higher up-
stream than downstream in these estuaries. Inverse estuaries are
found in Australia, Central America, the Gulf of California, the Middle
East, West Africa, and northern South-Asia; a similar effect occurs
with sea-ice formation in high latitudes (Nunes-Vaz, 2012).
There are three major natural water quality factors that affect any
transitional water body: dissolved oxygen (DO); salinity; and, sedimen-
tation. As noted above, sills can reduce bottom water DO as can reduced
flow or water circulation. Salinity can vary vertically, horizontally, and
seasonally. Sedimentation from upstream or downstream can change
transitional waters into meromictic lakes (i.e., with an upper freshwater
layer and deeper more saline layers, in some cases hyper-saline bottom
water layers). In addition to the above three major factors, transitional
waters also tend to have strong gradients in temperature, pH, redox po-
tential (Eh), and nutrients. These gradients can occur over any or all of:
upstream to downstream; laterally; and, vertically. Gradients can also
vary seasonally and will influence biogeochemical processes occurring
within transitional waters as discussed further later in this paper.
 P.M. Chapman et al. / Environment International 55 (2013) 71–91 73

Transitional water bodies are not steady-state systems; natural var-

iability is high in terms of both water chemistry and resident aquatic
fauna. In other words, change is the norm within transitional water
bodies. Given their high degree of spatial heterogeneity and complexity,
and high degree of habitat fragmentation (Dauvin and Ruellet, 2009), it
is challenging to determine whether effects to resident fauna are natu-
ral (i.e., within the relatively large range of natural variability) or related
to, for example, anthropogenic sediment contamination.

2.1.1. Summary
As noted by Chapman and Wang (2001), transitional waters are
dynamic, complex and unique systems. Potential effects of contami-
nated sediments cannot be fully assessed without understanding sea-
sonal and natural variability (i.e., stochasticity) and appropriately
bounding this variability.

2.2. Ecology of transitional waters

The standard paradigm for estuarine ecology (and by extrapolation,

for other transitional waters) has been that proposed by Remane
(1934), the “paradox of brackish water”, where transitional waters
have fewer numbers of taxa than fresh or marine waters (Fig. 1A). Spe-
cifically, diversity of freshwater taxa declines rapidly as salinity in-
creases, with minimum taxa richness at salinities of about 5 to 7.
Brackish water taxa dominate from about 7 to 17 salinity, after which
the diversity of marine taxa increases. This paradigm is based on the un-
stable and unpredictable nature of transitional water bodies, which ren-
der them difficult habitats for biota, particularly given wide spatial and
temporal variations in salinity in some transitional waters.
Whitfield et al. (2012) reviewed this paradigm and noted that it
is based solely on studies in the Baltic Sea and appears to be primarily
applicable to an open brackish sea and its river mouths, not to estuar-
ies or coastal lagoons. They also noted that there are freshwater taxa
that can survive in relatively high salinity waters and marine taxa that
can survive in relatively low salinity waters. They suggest that brack-
ish water fauna can survive and thrive in a wider range of salinity
conditions than suggested by Remane (1934) and that other factors
than salinity can influence taxa presence, abundance, and distribution
(e.g., sediment type for benthic infaunal communities which, in sedi-
ments of low permeability and high porosity, are exposed to different Fig. 1. Paradigms of transitional waters taxa distributions. A. Remane's (1934) “paradox of
brackish water”. B. Whitfield et al.'s (2012) new conceptual model.
pore (interstitial) water salinities than the overlying waters — Chapman,
1981). Remane's (1934) Artenminimum (species minimum) paradigm
has also been challenged in the Baltic Sea (Schubert et al., 2011). assessing resident communities and where there are more marine
Whitfield et al. (2012) propose a revised conceptual model for es- than freshwater and transitional taxa.
tuarine biodiversity related to salinity that we have applied to transi-
tional waters in general (Fig. 1B). The three key concepts are: more 3. Assessment techniques: chemistry
marine than freshwater taxa; less penetration by freshwater taxa
into more saline regions than by saltwater taxa into less saline re- Chemical analyses typically provide an initial line of evidence (LOE)
gions; and, transitional water taxa (neither fresh nor marine) are that is ultimately used with other LOE in a weight of evidence (WOE)
less abundant than marine taxa. Benthic infaunal distributions will assessment. Although not specifically described below, the chemistry
vary with seasonal or other shifts in salinity and can cover distances LOE can include bioaccumulation assessments using living organisms
of many kilometers (Chapman and Brinkhurst, 1981). Benthic infau- and/or passive sampling devices — such assessments are conducted
nal distributions will also vary with sediment type, and other factors similarly in fresh, marine and transitional waters (Maruya et al., 2012)
including hypoxia. and are thus not further discussed herein.
Naturally variable and hence stressful water quality conditions in
transitional waters can be challenging for many taxa, and resident 3.1. Unique processes and dynamics
taxa may be energetically challenged by these conditions. In some
cases cycles of mortality and recolonization may occur (Chapman and As an interface between land and the ocean, transitional waters re-
Wang, 2001), particularly where natural salinity and water quality var- ceive chemical contaminants primarily via riverine input, atmospheric
iations are extreme, for instance temporarily open/closed (naturally or deposition, and direct or indirect discharge of agricultural, municipal
artificially) estuaries. and industrial wastes. Some of the wastes will be transported to the
open ocean, with the rest degraded in transitional waters or ultimately
2.2.1. Summary stored in the sediments. As in other aquatic systems, sediments in tran-
The conceptual model for transitional waters (Fig. 1B) provides sitional waters can act as sources or sinks for chemical contaminants,
the basis for determining appropriate toxicity test taxa and for depending on inputs from external sources, in situ processes in the
74 P.M. Chapman et al. / Environment International 55 (2013) 71–91
water column, and post-depositional diagenetic alterations in sedi-
ments including bioturbation (De Backer et al., 2011).
Bioavailability of sediment contaminants varies with sediment
properties (Campana et al., 2012), and is controlled by their binding
phases in the sediments (e.g., iron and manganese oxyhydroxides,
sulfides, and organic matter for trace metal contaminants; organic
carbon for non-polar organic contaminants; Chapman and Wang,
2001). Quantitative assessment of bioavailability and toxicity based
on chemical measurements of the contaminant and its binding phases
is challenged in transitional waters by spatial and temporal heteroge-
neities in biogeochemical processes that govern the transport and
transformation among the dissolved phase, suspended particle phase,
and bed sediment phase (Fig. 2). For instance, reductions in bottom-
water DO concentrations can significantly increase the dissolved fraction
of some metals within contaminated sediments over short time periods
and their release from sediments over longer time periods (Banks et al.,
2012a, 2012b). Cyclic changes in overlying water pH and salinity can dra-
matically influence metal release from sediments in transitional waters
(Hong et al., 2011). Arguably no biogeochemical processes are unique
to transitional waters; what is unique, however, is how these processes
are influenced by and coupled to the exceptional dynamics of suspended
particles and to the changes in salinity (Fig. 2), as detailed below.
3.2. Role of suspended particles
Sediments in transitional waters are derived from continental and
coastal erosion, atmospheric deposition, in situ chemical and biological
processes, and human activities. Coarse sediments (e.g., sands, gravel)
settle to the bottom and become bed sediments, which generally move
slower than the mean flow of water via saltational processes along the
sea bed (Bianchi, 2007). The majority of sediments (up to 99%: Bianchi,
2007; Syvitski et al., 2000) transported to transitional waters are, howev-
er, fine particles (e.g., clays, silts, colloidal aggregates) and seston (bio-
genic entities such as microorganisms, zooplankton, phytoplankton)
that can stay suspended in the water column for a prolonged period of
time.
Fig. 2. Transport and partitioning processes of chemical contaminants in transitional
waters among the dissolved (CD), suspended particles (CSP), bed sediments (CS) and
sediment pore water (CPW) phases. Of critical importance are the dynamics of
suspended particles (sedimentation/resuspension, particulate organic matter (POM)
production/remineralization) and gradients in salinity. The terms “sorption” and
“desorption” are loosely used here to include any processes that result in the associa-
tion of the chemical to or removal from suspended particles, respectively. Not depicted
in this diagram are degradation of the chemicals and interactions with biota.
Although suspended particles can move relatively closely with
water flow (Bianchi, 2007), they are involved in a dynamic state of ex-
change with bed sediments, particularly in transitional waters where:
re-suspension of bed sediments is enhanced by tide-, wind- or river
flow-induced turbulence, as well as by bioturbation; and, sedimenta-
tion of suspended particles is enhanced by increased flocculation and
coagulation due to destabilization of repulsive electrostatic forces by
high salinity. Transitional waters such as estuaries, with their salinity
gradients and tidal movements, “represent gigantic natural coagulation
reactors where much of the dispersed colloidal matter of rivers settles”
(Stumm and Morgan, 1996); coagulation processes in transitional wa-
ters can rival those of wastewater systems (Bianchi, 2007). For instance,
aggregation of metal-containing nanoparticles occurs in transitional
waters, decreasing (though not diminishing) bioavailability of metals
associated with those nanoparticles (Khan et al., 2012).
In addition to the resuspension/sedimentation cycle, particulate
organic matter (POM), which is the organic matter (OM) fraction of
suspended particles or bed sediments, also undergoes the production/
remineralization cycle (Fig. 2). POM in transitional waters can origi-
nate from both riverine and coastal ocean end-members from autotro-
phic (primarily photosynthesis, but chemosynthesis has also been
reported in OM-enriched estuaries; McLeod et al., 2010) and hetero-
trophic production which fix OM from inorganic carbon and nutrients.
Depending on the lability of POM, sedimentation rate, and redox con-
ditions, a considerable fraction of POM (10–90%) can be buried and
preserved in bed sediments below the active zone of diagenesis
(Bianchi, 2007), while the rest of the POM is remineralized to inorgan-
ic nutrients via microbially mediated oxidation processes.
Suspended particles in transitional waters may occur as discrete enti-
ties, but more often as assemblages with a relatively inert silicate core
surrounded by a more reactive coating comprising iron and manganese
oxides, carbonates, sulfides, detrital OM and microorganisms (Turner
and Millward, 2002). This coating is highly reactive to ionic or polar con-
taminants via surface adsorption and/or co-precipitation, and to neutral
or non-polar organic chemicals via hydrophobic sorption (Stumm and
Morgan, 1996). For simplicity, we loosely refer to all these processes
resulting in the bonding or association of a contaminant to suspended
particles as “sorption”. As shown in Fig. 2, once sorbed on suspended par-
ticles, contaminants can be released back to the dissolved phase
(“desorption”), or transported to bed sediments where they can further
exchange with pore water. Transport between contaminants in sediment
pore water and the overlying water occurs via molecular diffusion, bio-
turbation, or bioirrigation (Boudreau and Jorgensen, 2001).
The distribution coefficient below has been commonly and conve-
niently used in describing the partitioning between contaminants in
dissolved and particulate form:
KD ¼ CSP =CD ; ð1Þ
where CSP and CD are the equilibrium concentrations of the contami-
nant of concern in suspended particles and in the dissolved phase, re-
spectively. However, KD is rarely a constant, especially in transitional
waters where large gradients exist spatiotemporally in pH, salinity,
temperature, and in the concentrations of suspended particles. Fur-
thermore, the dissolved and sorbed phases of a contaminant are rarely
at a thermodynamic equilibrium in transitional waters because of: the
relatively slow kinetics of sorption/desorption compared with flushing
times; or, the instantaneous addition or removal of suspended particles
due to the aforementioned sedimentation/resuspension or production/
remineralization processes (Turner and Millward, 2002).
3.3. Role of salinity
As pointed out by Chapman and Wang (2001), the partitioning of a
contaminant among the dissolved, particulate, and bed sediment phases
in transitional waters is further complicated by spatiotemporal changes
 P.M. Chapman et al. / Environment International 55 (2013) 71–91
in salinity. For neutral or non-polar organic contaminants, sorption onto
suspended particles or sediment (primarily POM) typically increases
with increasing salinity due to a coupled salting-out — sorption
mechanism (Turner and Millward, 2002; Turner and Rawling, 2001).
The salting-out effect refers to the decrease in the aqueous solubility of
non-polar or weakly polar organic compounds with increasing ionic
strength (Schwarzenbach et al., 2002). Although quantitative under-
standing is limited, the salting-out effect in transitional waters can
be envisioned as the tight binding of major salt ions (e.g., Na +, Cl−) to
water molecules, which reduces the “freedom” of some water mole-
cules to solvate nonpolar chemicals (Schwarzenbach et al., 2002), en-
hancing sorption onto POM. The partitioning of non-polar chemicals
on POM in high salinity waters is further favored as the hydropho-
bicity of POM generally increases with increasing salinity (Turner
and Rawling, 2001). An opposite, salting-in effect could also occur for
some organic compounds, but has rarely been observed in transitional
waters.
For metal contaminants (including metalloids and non-metals), the
combined effect of complexation and competitive adsorption with sea-
water ions tends to decrease their sorption onto suspended particles
with increasing salinity (Turner and Millward, 2002). Complexation
by seawater anions (e.g., Cl−, SO42−), for instance, increases the solubil-
ity of many metals by forming soluble complexes. Seawater cations
(e.g., Na +, K +) or anions (e.g., Cl−, SO42−) can compete with metal cat-
ions (e.g., Cd 2+, Pb2+) or oxyanions (e.g., CrO42−, SeO42−, AsO33−) for the
binding sites on suspended particles. However, a growing body of liter-
ature has shown that a salting-out effect similar to that for non-polar
compounds can also occur in transitional waters to trace metals that
bind strongly with organic ligands (e.g., Cr, Cu, Hg, Ni, Pb, Pd, Zn; but
not Cd) (Cobelo-Garcia et al., 2008; Turner et al., 2002, 2004a, 2004b).
This effect is attributed to the formation of hydrophobic metal com-
plexes with dissolved organic ligands which then behave similarly to
non-polar organic compounds in transitional waters (Turner et al.,
2004a).
3.4. Non-conservative mixing of contaminants in transitional waters
Consider a simple one-dimensional transitional water body with
only two end members, one being freshwater and the other seawater.
If a chemical behaves conservatively (i.e., not being produced or con-
sumed) during mixing, at steady state its dissolved phase concentra-
tion would vary linearly with salinity (Fig. 3A) and its particulate
phase concentration would vary curvilinearly with salinity (Fig. 3B;
the actual shape of the curve depends on the relative concentrations
of suspended particles in freshwater and seawater). Such conserva-
tive mixing, however, rarely occurs in transitional waters. Due
to the aforementioned salinity- and suspended particle-dependent
partitioning of contaminants in transitional waters, along with trans-
formation and degradation, the mixing of most contaminants in tran-
sitional waters deviates from the conservative mixing curves. Instead,
the dissolved or particulate concentration of a contaminant may ex-
hibit addition-like or removal-like patterns with salinity (Fig. 3), or
both at different sites in the same transitional water body.
A similar concentration–salinity distribution pattern does not di-
rectly apply to surface sediments where the mixing regime is very dif-
ferent. Nevertheless, the distribution patterns of a contaminant in the
water column can offer insights into whether the bed sediments act
as a source or sink for that contaminant. For instance, when both
the dissolved and particulate concentrations of a contaminant show
an “addition” pattern, very likely there is a net flux of the contami-
nant remobilized from the surface sediments.
3.5. Cautions
Chemical assessment techniques for contaminated sediments typi-
cally involve measuring concentrations, and better still speciation, of
75
potential contaminants in sediments or biota and comparing them
with established or inferred benchmark values deemed appropriate
for the specific assessment purposes. When properly used in conjunc-
tion with biological LOE (e.g., bioindicators, biomarkers; see sections
below), chemical assessment techniques are a powerful tool to screen
contaminants of primary concern, to apportion sources of contamina-
tion, and to establish targets for remediation.
Cautions are, however, warranted when applying existing chemical
assessment techniques and benchmark values, many of which were de-
veloped for freshwater or marine systems, to transitional waters, due to
the aforementioned unique dynamic nature of salinity and suspended
particles and associated contaminant processes. To account for such
complex biogeochemical processes, chemical assessment techniques
for transitional waters can be highly resource demanding and the inter-
pretation of the results can be challenging. For instance, where and when
to collect sediment samples from a transitional water poses the first
major challenge in obtaining meaningful chemical measurements that
are “representative” of the system. The dynamic exchange of chemicals
between suspended particles and bed sediments implies that both
suspended particles and bed sediments need to be chemically assessed.
Further, as noted by Bay et al. (2012) “bulk chemistry measurements
do not address bioavailability and thus are unable to accurately predict
changes in organism exposure resulting from geochemical factors.”
Maruya et al. (2012) agree and note further that such measurements
do not provide accurate depictions of organism exposure nor do they
provide useful information for determination of causality.
Although benchmark values, such as sediment quality values (SQVs;
Chapman et al., 1999), are available under various jurisdictions for
many chemical contaminants, they were developed almost exclusively
for freshwaters or salt waters. Direct comparison of a chemical mea-
surement to the corresponding SQV has often been problematic even
in freshwaters or salt waters where the SQV was derived (Chapman
et al., 1999); application of those SQVs to transitional waters without
biological LOE should be totally discouraged. There is thus a need to devel-
op sediment benchmark values for transitional waters, although such de-
velopment will require a very different strategy to account for the reality
that speciation and bioavailability vary with salinity and with resident
biota at a specific salinity — one value or one curve does not fit all.
3.6. Summary
Chemical assessments (measuring concentrations or speciation of
contaminants in sediments and comparing them to appropriate bench-
marks) have three uses: screening contaminants of primary concern;
apportioning sources of contamination; and, establishing remediation
targets based on this and other LOE combined in a WOE assessment.
There are four primary cautions related to these uses due to the unique,
dynamic nature of salinity and suspended particles, and associated con-
taminant processes noted above: determine when and where to sample
to obtain “representative” sediment samples in spatio-temporally dy-
namic transitional waters; account for the reality that speciation and
bioavailability vary with salinity and with resident biota at the specific
salinity; determine appropriate benchmark values, which may be a
range of values rather than a single value (use marine or freshwater
benchmarks for screening with caution in transitional waters, recogniz-
ing that uncertainty can be high); and, assess suspended particles and
dissolved contaminants, due to their dynamic exchange with bed
sediments.
4. Assessment techniques: bioindicators
Bioindicators are whole organism responses used to measure po-
tential effects of stressors on populations or communities of organ-
isms. Sediment-dwelling or associated biota in transitional waters
are part of a complex food web that changes seasonally (e.g., nursery
areas for juvenile marine fish in spring; rearing and feeding areas for
76 P.M. Chapman et al. / Environment International 55 (2013) 71–91

Fig. 3. Distribution patterns of a chemical as a function of salinity in the water column of a two end-member (freshwater and seawater, in which the concentration of the chemical is
denoted CFW and CSW respectively), steady-state transitional water system. A) Dissolved concentrations. B) Particulate concentrations.
Panel A is after Wen et al. (1999).

those fish later in the year; summer algal blooms), with trophic levels
fluctuating in space and time (Vinagre et al., 2012). As previously
noted, physico-chemical conditions in transitional waters are variable
in time and space, which will directly and indirectly affect the bioavail-
ability and toxicity of contaminants in sediments, i.e., both chemically
and in terms of additional energetic stress on exposed organisms.
4.1. Toxicity tests
Toxicity tests should encompass both acute (survival) and sublethal
endpoints (growth, reproduction, behavior and other biomarkers of
effect — see Section 5) using at least two (Greenstein and Bay, 2012)
and ideally three or four appropriately sensitive, standardized
sediment-dwelling and/or sediment associated test organisms that are
reasonably similar to those found (or expected to be found) at a sedi-
ment site based on available data (Chapman and Anderson, 2005;
Chapman and Smith, 2012; Environment Canada Ontario Ministry of
the Environment, 2008). Toxicity tests involving only one test organism
rather than tests involving several different test organisms should not
be relied on given differences in species sensitivities to different chem-
ical stressors (Anderson et al., 2008; McPherson and Chapman, 2000).
Greenstein and Bay (2012) provide useful guidance in evaluating toxic-
ity tests relative to the following factors: organism availability; method
description; technical difficulty; concordance of responses; relative
sensitivity; variability among and within laboratories; precision;
confounding factors; and, cost.
Toxicity testing with whole organisms should focus on whole sed-
iments that have been appropriately characterized (i.e., grain size,
pore water salinity) to allow appropriate choice of test species with-
out undue manipulation of the test sediments (e.g., without changing
the salinity and thus contaminant bioavailability to suit particular test
species). It is critically important to measure and match natural salin-
ity conditions rather than ignoring them and/or imposing arbitrary
salinity conditions. Both pore and overlying water salinities should
be measured at the start and end of testing. Ideally overlying water
toxicity should be tested in conjunction with sediment toxicity tests
to quantify the relative contribution of each to any observed toxicity
(Hose et al., 2006). Sieving to remove the possibility of biological in-
terferences with indigenous organisms (Fisher et al., 2004), if neces-
sary, must be done without unduly changing pore water salinities.
Field collections of organisms for sediment toxicity testing need to
consider confounding factors. For instance, differences in tolerance to
natural stressors are possible between different populations from
transitional waters. For some organisms, collections undertaken at
different times of the year may provide animals with different energy
characteristics (e.g., different growth rates — Scarlett et al., 2007). As
noted by Chapman and Wang (2001), toxicity testing of sediments in
transitional waters needs to occur with a reasonable knowledge of
the ecology of those waters and the potential range of pore water
 P.M. Chapman et al. / Environment International 55 (2013) 71–91
salinities, avoiding “a snapshot in time of a dynamic and unique
system”.
Chapman and Wang (2001) divided single-species estuarine tox-
icity tests into two categories: tests adapted to estuarine conditions;
and, tests designed for those conditions. This division was based on
Remane's (1934) “paradox of brackish waters” which, as previously
noted, appears to no longer be applicable to transitional waters.
Thus, we no longer believe that those categories have any import;
rather, the focus should be on salinity and grain size tolerance, and
test endpoints.
Table 1 summarizes information on transitional water toxicity
tests developed and published since the review by Chapman and
Wang (2001). Readers are referred to that earlier publication for in-
formation on those earlier tests. Some interesting observations can
be made comparing the earlier and present reviews. First, the impor-
tance of salinity in conducting sediment toxicity tests in transitional
waters is now recognized. Second, testing remains weighted to crus-
taceans, in particular amphipods. Chapman and Wang (2001) listed
19 different estuarine sediment test taxa of which 12 were crusta-
ceans (8 amphipods), a fish, a polychaete, four molluscs, and a bacte-
rium. We list 24 different estuarine sediment test taxa of which 13 are
crustaceans (9 amphipods, 3 copepods, 1 crab), a polychaete, 4 mol-
luscs, 1 chironomid, 3 benthic diatoms, a protozoan, and a microalga.
Third, the lack of the genus Corophium in transitional water tests has
now been rectified. Corophium volutator is the most commonly used
species of this genus for a variety of endpoints. It also appears to be
appropriate and sensitive for future behavioral sediment toxicity as-
sessment (Kirkpatrick et al., 2006). Fourth, the lack of insects such as
chironomids, which are found in transitional waters (Williams and
Williams, 1998), or oligochaetes in sediment toxicity tests in these
waters has only been partially rectified. In fact, the list of estuarine
test species still remains relatively small (12 species in Chapman and
Wang (2001) not included in Table 1: 1 fish, 7 crustaceans, 1 poly-
chaete, 2 molluscs, 1 bacterium). However, per Fig. 1, the list of possi-
ble test species can be extended by including saltwater and, to a lesser
extent, freshwater species where and when appropriate — with the re-
peated caution that pore water salinities need to be determined before
choosing test organisms. Table 1 also does not include toxicity tests
involving only biomarkers where fish, crustaceans and molluscs
(mainly marine species) are commonly used. To date toxicity tests
have been largely laboratory-based rather than conducted in situ in
the field, where they may arguably provide more ecologically realistic
(but more difficult to interpret) information.
4.1.1. Summary
Guidance is provided regarding sediment toxicity tests in transi-
tional waters. Testing should involve more than one organism,
encompass both acute and sublethal endpoints, measuring and
matching natural salinity conditions rather than ignoring them or im-
posing arbitrary salinity conditions.
4.2. Biological surveys
Benthic infaunal communities in transitional waters can exhibit
symptoms of disturbance without anthropogenic influence given
the extreme physical and chemical stresses in such waters. Organisms
burying into muddy sediments are not directly affected by overlying
water salinities but rather by pore water salinities, which change
much more slowly in muddy than in sandy sediments; seasonal var-
iations in pore water salinities can result in seasonal shifts in benthic
infaunal distributions (Chapman and Wang, 2001). Organism life-
styles including avoidance and use of micro-environments may result
in their unexpected association with contaminated sediments (Rubal
et al., 2011).
Biological surveys in transitional waters need to be conducted in
the context of natural changes over time and space in both physical
77
and chemical conditions and of resident biota. Reference comparisons
are typically not realistically possible (Barbone et al., 2012); gradient
approaches are necessary but with recognition of the uncertainty due
to multiple confounding factors in transitional waters. Pore water sa-
linities must be determined as must pore water and groundwater
flows in permeable sand sediments (Santos et al., 2012).
Temporal changes in community composition may, in addition to
changes in physical and chemical conditions (e.g., changes in nutrient
cycles due to climate change — Jarvie et al., 2012; changes in salinity
due to climate change — Schlenk and Lavado, 2011), reflect the arrival
and establishment of invasive species related to global climate
change. Interactions between native and invasive species can be com-
plex. For instance, the native crab Carcinus maenas can facilitate the
invasion of the mussel Xenostrobus secures as it preys preferentially
on the native mussel, Mytilus galloprovincialis (Veiga et al., 2011). In-
vasive or introduced species can affect major ecosystem changes par-
ticularly when the non-native species is a functionally novel invader,
which can include closely related species (Benjamin and Baxter,
2012).
Ecological stress, from any source, is best measured using multiple
variables, methods or analyses and not necessarily limiting these to
the same or a few assumptions (see Integrative Assessments, Section
6). Sufficient data are required to adequately determine different habi-
tats within transitional waters based on biotic interactions (competi-
tion, predation) and physico-chemical factors (e.g., salinity,
sedimentation, DO, temperature) unrelated to chemical contamination.
These different habitats and their status will be specific to individual
transitional waters and will likely change over time and space; howev-
er, habitat usage patterns may, in some cases, be common to more than
one transitional water body (Ferraro and Cole, 2012).
In transitional water bodies the effects of climatic variability and
the highly variable water quality characteristics of those water bodies
mimic effects due to chemical stressors, making it difficult to distin-
guish chemical stressor effects on benthic infaunal communities
from natural variability (Veríssimo et al., 2013). This is the “Estuarine
Quality Paradox” described by Elliott and Quintino (2007), who noted
that estuarine biota, because they are exposed to dynamic, diversi-
fied, and changing water quality conditions, likely have a relatively
high degree of tolerance/adaptation. This tolerance/adaptation poses
an additional constraint when attempting to determine ecosystem
status from biological responses and when assessing cause–effect
relationships between contaminants and biological endpoints amidst
a complex pool of stressors. Thus, biological surveys of transitional
water bodies must identify and, to the extent possible, quantify the
effects of stressors other than anthropogenic chemicals on the ben-
thic infauna. Mesocosms can be useful in this regard (O'Brien and
Keough, 2013).
Key determinations during community structure evaluations in-
clude any changes to keystone bioturbators (e.g., removal of those
taxa) that could induce large changes in habitat structure with cas-
cading impacts on other sediment-dependent organisms (Meysman
et al., 2006), as well as affecting contaminant bioavailability. Sedi-
ment burial occurs naturally in transitional water bodies; however,
resident taxa typically exhibit mechanical and/or physiological adap-
tations to survive natural deposition events (Hinchey et al., 2006).
Sampling effort is arguably the most important metric in deter-
mining the status of biological communities in transitional waters.
The appropriate sampling effort is “the level at which the addition
of another sampling unit of effort does not substantially increase spe-
cies richness or change proportional abundances” (Gamito et al.,
2012). In the case of benthic infaunal communities sieve size is
more important than sample area to determine species richness and
abundance but must be balanced against level of effort required in
terms of sample processing time — in some cases a 1.0-mm sieve
may provide sufficient information without the need for a smaller
sieve size (Hammerstrom et al., 2012).
78 P.M. Chapman et al. / Environment International 55 (2013) 71–91

Table 1
Transitional waters sediment toxicity test organisms. Single species, whole sediment exposures, and sediment-overlying water exposures. Unless otherwise noted, laboratory testing.
Testing involving only biomarkers excluded.

Test organism Salinity tolerance Grain size tolerance Endpoints Comments References

Whole sediment exposures

Chironomid, 0–10; highest Not established 48-h in situ sediment exposure, Laboratory cultured Soares et al. (2005)
Chironomus salinity only at flood 1-h post-exposure feeding
riparius tide; otherwise, b2
Amphipod, 9–25 for survival “Sand or mud”; builds 10-d survival Field collected; reburial and emergence not Marsden and Wong
Paracorophium tubes useful endpoints (2001)
excavatum
Amphipod, Melita 5–35 over 28 d for “Silty to silty-sand” 10-d survival; 28-d survival, Field collected; lower temperatures delay Hyne et al. (2005)
plumulosa survival; 10–25 over growth, fertility maturation, reduce fertility [Can be laboratory
28 d for fertility and cultured — require
growth supplemental food
(Hyne et al., 2009)]
Tests conducted 42-d survival, gravidity, fertility, Laboratory cultured Gale et al. (2006)
at 25 growth, bioaccumulation
Not specified 13-d reproduction: Laboratory cultured Mann et al. (2009)
gametogenesis, fertilization,
embryo development
Tests conducted 10-d survival and reproduction Simpson and
at 30 Spadaro (2011)
Amphipod, “Wide range”; tests “Wide range”; live in Full life-cycle; 42-d survival, Laboratory cultured; individual-level Manyin and Rowe
Leptocheirus conducted at 13 open tubes growth, reproduction bionergetic measurements related to (2006)
plumulosus population-level effects
Amphipod, 10–25 for chronic Not established; builds 49-d survival, growth, Field collected; chronic endpoints highly van den
Corophium endpoints; 4–40 for tubes, should have reproduction sensitive to ammonium and nitrate Heuvel-Greve et al.
volutator survival relatively wide (2007)
Not established, see tolerance 28-d survival, growth; ≈75 d Field collected; studies conducted at different Scarlett et al.
above survival, growth, reproduction times of the year may not be comparable — (2007) [additional
collect in summer information in
Peters and Ahlf
(2005)]
Amphipod, Not established; Wide range, clean 10-d survival, 21-d survival and Laboratory cultured; increased temperature Castro et al. (2006)
Corophium typically found in gravel to 96% fines fecundity increases toxicity and Ré et al. (2009)
multisetosum lower salinities 10-d survival Field collected Ré et al. (2007)
to 22
Amphipod, 19–35 for survival Wide range so long as 10-d survival Field collected Melo and Nipper
Tiburonella some medium and (2007)
viscana coarse sand present
Amphipod, >20 for testing “Can be used for 28-d survival, growth, Costa et al. (2005)
Gammarus although some testing all sediment reproductive traits and Neuparth et al.
locusta populations live at types” (2005)
5–7
Copepod, Not established Not established; tested 96-h LC50 Laboratory cultured; gender-specific Hagopian-Schlekat
Amphiascus in “muddy” sediments differences (males smaller than females) et al. (2001)
tenuiremis
Copepod, Not established, Not established 24-d survival, fecundity, clutch Laboratory cultured; reproductive endpoints Hack et al. (2008)
Robertsonia tested at 32; size per female, number of eggs, the most sensitive
propinqua considered “marine juvenile survival
species”
Copepod, Nitocra “Can adapt to a wide Not established; 4-d survival, 7-d development Laboratory cultured Perez-Landa and
spinipes range of salinities”; testing conducted in Simpson (2011)
tested at 30 but can sediment and
be found at 7 water-only exposures
Sediment exposures 10-d survival and reproduction Simpson and
Spadaro (2011)
Mollusc, 4–30 for survival Not established 21-d: survival in sediment, Laboratory cultured; T. semidecussatus Byrne and
Scrobicularia survival in air, burrowing recommended for routine assessments O'Halloran (2001)
plana behavior, histopathology,
Mollusc, Tapes biomarkers, tissue metal
semidecussatus concentrations,
(=Ruditapes condition indices
philippinarum)
Mollusc 5–40 for survival Not established 48-h, post-exposure feeding In situ test; field collected organisms; Krell et al. (2011)
(mudsnail), temperature, salinity and silt content influence
Hydrobia ulvae post-exposure feeding
Protozoan, Not established Not established 8-h mortality, 24-h replication Laboratory cultured; screening tests to evaluate Gomiero et al.
Euplotes rate; endocytosis rate, lysosomal feasibility (2013)
crassus membrane stability
Benthic diatoms, Not established Test sediments 72-h growth Laboratory cultured; low sensitivity to tested Moreno-Garrido
Cylindrotheca primarily “sandy”; silt sediments et al. (2007)
closterium, inhibits growth
Phaeodatylum
tricornutum,
Navicula sp.
 P.M. Chapman et al. / Environment International 55 (2013) 71–91 79

Table 1 (continued)
Test organism Salinity tolerance Grain size tolerance Endpoints Comments References

Sediment-overlying water exposures

Amphipod, 0–10; survival low Not relevant; water 10-d survival and growth Laboratory cultured Werner et al.
Hyalella azteca above ≈ 7 testing only (2010)
Amphipod, “Wide range” Not applicable; water 96-h acute lethality, 1-h and Field collected Hecht and Boese
Eohaustorius only exposures 48-h reburial (2002)
estuarius
Polychaete, Tolerant to “great Contained in assay 48-h and 96-h LC50 survival; In situ test; field collected organisms; higher Soares et al. (2005)
Hediste fluctuations” but chambers but 48-h IC50 post-exposure feeding; feeding at higher temperatures and Moreira et al.
diversicolor these influence tolerated wide particle 20-d IC20 growth (2005, 2006c)
post-exposure size range
feeding (63–2000 μm)
Bivalve, Mulinia Not established Not established To 30-d post-spawning: survival, Laboratory cultured Cripe (2006)
lateralis growth
Crab, Carcinus 10–35; feeding rate Not applicable; 48-h exposure, 30 min In situ test; field collected organisms; higher Moreira et al.
maenas higher at 35 than 10 contained in assay post-exposure feeding relative to feeding at higher temperatures; seasonal (2006a)
chambers reference(s) physiological differences influence contaminant
sensitivity (Dissanayake et al., 2011)
Microalga, Tolerant to “wide Not applicable; 6–8 d mean specific growth In situ test; laboratory cultures Moreira et al.
Phaeodactylum salinity fluctuations” sediment overlying rate/d (2006b)
tricornutum water test

As previously discussed, changes in water and sediment quality will
occur naturally across time and space in transitional waters, requiring ap-
propriate multivariate trend detection and temporal pattern recognition.
Veríssimo et al. (2013) recommend screening application of Min/Max
Auto-correlation Factor Analysis based on Principle Component Analysis
taking into account serial auto-correlation of time series with no a priori
assumptions regarding potential trends. More robust approaches such
as Canonical Correspondence Analysis and Multidimensional Scaling
can then be applied based on the hypotheses generated from this initial
multivariate screening step. As noted by Chapman (1996) both univariate
and multivariate approaches provide useful information; however, pre-
scriptive recommendations for statistical analyses are not realistically
possible other than to recommend a priori involvement of a qualified
and experienced biostatistician.
4.2.1. Summary
Natural changes occur in transitional waters over time and space in
both physical and chemical conditions and resident biota; it is critically
important to bound stochasticity. Different habitats within transitional
waters should be determined based on biotic interactions and physico-
chemical factors unrelated to chemical contamination. Reference
comparisons are generally not realistically possible; use gradient ap-
proaches but recognize uncertainty due to multiple confounding
factors; determine pore water salinities and groundwater flows in per-
meable sand sediments; use an appropriate level of sampling effort and
balance sieve size against processing time and resulting data needs;
expect the arrival and establishment of invasive species; and, measure
stress using multiple variables, methods, or analyses following the
advice of a qualified and experienced biostatistician.
5. Assessment techniques: biomarkers
Biomarkers serve as an exposure and/or effect LOE in assessments
of environmental quality in transitional and other waters (Benedetti
et al., 2012; Chapman and Hollert, 2006; Galloway et al., 2004;
Hagger et al., 2009; Morales-Caselles et al., 2008, 2009; Piva et al.,
2011; Riba et al., 2004). They are specific biological responses mea-
sured within individual organisms, ranging from molecular through
cellular, metabolic and physiological responses to behavioral changes.
Biomarkers are measured inside an organism in body fluids, cells or
organ tissues, or in its products (e.g., blood, hepatopancreas, digestive
gland, liver, kidney, gonads, gills, urine, feces); they indicate changes
from normal conditions due to a stressor, which can be a chemical toxi-
cant (van der Oost et al., 2003). They can be measured for organisms
subjected to toxicity testing under controlled laboratory conditions
and/or in situ in the field (Martín-Díaz et al., 2004, 2008a; Morales-
Caselles et al., 2008, 2009; Piva et al., 2011), or can also be determined
on sampled resident aquatic organisms (Costa et al., 2013; Erk et al.,
2011; Oliveira et al., 2009; Serafim et al., 2012).
The key advantage of biomarkers is the fact that they can, if used cor-
rectly, provide early warning of contaminant exposure or of potential
adverse effects to individuals (Picado et al., 2007), that may translate
to population-level effects, although determination of the latter typical-
ly requires additional LOE. Biomarkers can also be used to assist in de-
termining cause-and-effect, linking the bioavailability of chemicals
(i.e., their concentrations at target organs) with biological processes
(Galloway et al., 2004). Some biomarkers are specific to certain groups
of chemicals, others are not; thus, some authors classify biomarkers as
specific or non-specific (Monserrat et al., 2007). Specific biomarkers
are particularly useful (Chapman, 2007; Galloway et al., 2004; Martín-
Díaz et al., 2004; Monserrat et al., 2007).
Biomarkers can be subdivided into three classes (Martín-Díaz
et al., 2004; NRC, National Research Council, 1987; Stahl et al., 2010;
van der Oost et al., 2003; WHO, World Health Organization, 1993)
(Fig. 4):
• Biomarkers of exposure cover the detection and the measurement
of an exogenous substance or its metabolite or the product of an in-
teraction between a xenobiotic agent and some target molecule or
cell that is measured in a compartment within an organism. These
biomarkers can be used to determine contaminant bioavailability,
providing a link between external concentration and internal
dose. They do not provide any insight into the susceptibility of ani-
mals to a specific disease state and by themselves do not necessarily
provide any indication of the increased risk that the organism may
experience as a result of the exposure.
• Biomarkers of effect include measurable biochemical, physiological
or other changes within tissues of body fluids of an organism that
can be recognized as associated with an established or possible
health impairment or disease. They in some instances reflect modi-
fications in the organism that precede actual structural or functional
impairment and can be used as early warning of potential
organism-level effects. However, many biomarkers of effect are
not associated with exposures to specific chemical agents.
• Biomarkers of susceptibility indicate the inherent or the acquired
ability of an organism to respond to the challenge of exposure to a
specific xenobiotic, including genetic factors and changes in recep-
tors that alter the susceptibility of an organism to that exposure.
They help to elucidate variations in the degree of responses to
80 P.M. Chapman et al. / Environment International 55 (2013) 71–91
Fig. 4. The three classes of biomarkers relative to the continuum from initial exposure to organism-level effects, in this case termed “disease”. Examples of biomarkers applied to
transitional waters are shown in italics.
Adapted from NRC (National Research Council) (1987) and Sumner and Fennell (2007).
stressor exposure observed between different individuals and are
useful in helping to determine the susceptibility of an individual
to manifest a toxic response or to develop a specific disease state.
These classifications are used inconsistently in the scientific liter-
ature since biomarkers of exposure and those of effect are distin-
guished by the way they are used (Martín-Díaz et al., 2004) and
since there is considerable overlap between each classification. For
example, blood or tissue contaminant concentrations, or metabolites,
may be used to estimate exposure. Altered enzyme activities may in-
dicate biologically effective doses, susceptibility, or preclinical effects,
while pathological lesions provide evidence of adverse consequences
(Galloway, 2006). Most biomarkers measure exposure to a stressor,
not organism-level effects from that stressor; still, some biomarkers
do measure effects that may translate to effects at the level of individ-
ual organisms (Chapman, 2007); these effects can be no-effect and
effect levels or time-to-response (Sumner and Fennell, 2007).
Biomarkers of exposure and effect are linked to biomarkers of sus-
ceptibility (cf. Fig. 4). Because of the difficulty in determining suscep-
tibility, the focus of field and laboratory investigations tends to be
only on biomarkers of exposure and effect (Stahl et al., 2010).
Tables 2 and 3 provide information regarding the most common
biomarkers of exposure and effects used to date within transitional
waters (including appropriate and inappropriate use), some of
which provide both measurements. The most common biomarker of
exposure is metallothionein (MT) induction which is not always in-
duced by metals; other stressors can induce MT, particularly in tran-
sitional waters possibly due to salinity variations and the existence
of complex mixtures of contaminants in sediments (Carreira et al.,
2013; Costa et al., 2012a). Monserrat et al. (2007) suggest the use of
the two enzymes that play a pivotal role in osmoregulation as bio-
markers to allow consideration of salinity interactions with both or-
ganism physiology and metal bioavailability: Na +–K +-ATPase and
carbonic anhydrase. These biomarkers could provide useful informa-
tion on salinity as a stressor in transitional waters.
Oxidative damage to lipids, DNA and proteins, and adverse effects
on antioxidant, enzymatic and non-enzymatic defense mechanisms
of aerobic organisms serve as key biomarkers of environmental
chemical contamination (Valavanidis et al., 2006), and have a history
of use in transitional waters (Benedetti et al., 2012; Costa et al.,
2011b; Liu et al., 2012; Oliveira et al., 2009; Serafim et al., 2012).
However, the whole-organism toxicological significance of oxidative
damage remains to be clearly evaluated, validated, and qualified
(van der Oost et al., 2003), particularly for contaminated sediments
(Martín-Díaz et al., 2008a; Morales-Caselles et al., 2008). Oxidative
stress biomarkers can be affected by factors external to contamina-
tion, for example by antioxidant defenses such as mucus secretion
(Monserrat et al., 2007).
Acetylcholinesterase (AchE) activity has proven to be a useful bio-
marker of organophosphorus pesticide exposure, particularly for verte-
brates (Galloway, 2006). Neuromuscular (e.g., AchE) and reproductive
biomarkers are related to behavior disruption in organisms exposed to
contaminants (e.g., swimming, feeding, locomotion, prey capture,
level of aggression). Behavior is a response at the level of the individual
organism that has clear links to effects at the population level through
alterations of survival or reproductive success (Amiard-Triquet, 2009).
However, these biomarker responses also vary with salinity in transi-
tional waters. For example, Pfeifer et al. (2005) found that different salin-
ities alone resulted in changes in AchE activity in the gills of Mytilus sp.
Many environmental contaminants, in particular estrogenic com-
pounds, have endocrine-disrupting properties. Impairments in reproduc-
tive capability may have a serious impact on affected populations in
transitional waters. Sensitive assays such as levels of vitellogenin are
promising, but their ecological significance remains to be established
(Barucca et al., 2006; van der Oost et al., 2003).
Physiological and morphological parameters comprise higher-
level responses that, following chemical and cellular interactions,
can be indicative of irreversible damage (van der Oost et al., 2003).
For example, histopathological biomarkers, although not specific to
particular contaminants or other stressors and whose use requires ex-
perienced researchers, provide useful information on the general
health of organisms, which can be related to the effects of exposure
to a variety of anthropogenic contaminants (Costa et al., 2011a; Riba
et al., 2004) and thus can be used in risk assessment (Costa et al.,
2012a). Qualitative/semi-quantitative histopathological approaches,
for example the relative weights of lesions and quantitative data,
can provide information on the biological significance of lesions
(Costa et al., 2009b) and support cause–effect assessments when
multiple toxicants are involved, as is typically the case in transitional
waters. Histopathology analysis also allows for assessment of the
presence of parasites, which can modulate pollution responses
(Paul-Pont et al., 2010). Histopathology is a major component of
biomonitoring programs in North America and Europe and is a powerful
tool to use when sampling feral organisms. Unfortunately, histopatho-
logical reference data on transitional water taxa are scarce, particularly
for aquatic invertebrates.
The use of immunotoxicology for risk assessment is a newly evolving
and challenging area. Although immunological injury can be a conse-
quence of chemical exposure, non-specific immune activity can also be
influenced by other external factors (Monserrat et al., 2007).
The use of genotoxicity biomarkers is growing. The involvement of
xenobiotic-metabolizing enzymes in carcinogenesis has been demon-
strated in some mammalian studies, which reported altered levels
and activities of these enzymes in preneoplastic and neoplastic le-
sions (Van der Oost et al., 2003). Damage to DNA can be one of the
most significant consequences of chemical insults to organisms
since this has the potential to affect not only individual organisms
but populations of organisms. The Comet assay provides a rapid
screening for potential DNA damage (Frenzilli et al., 2009; Picado
et al., 2007) compared to more laborious (but also more overall infor-
mative) methods than, for instance, sorting erythrocitic nuclear
abnormalities. However, confounding factors such as DNA repair ca-
pability and cell division rates obviate a clear relationship between
DNA damage and organism- or higher-level adverse effects (Costa
et al., 2011b).
Novel biomarker methodologies such as “omics” (transcriptomics/
toxicogenomics, proteomics and metabolomics — see Table 2) are in-
troducing new concepts for screening of exposure to contaminants
 P.M. Chapman et al. / Environment International 55 (2013) 71–91 81

Table 2
Biomarkers of exposure applied to transitional water environments.

Biomarker group Description Stressors triggering Appropriate use Disadvantages Reference

response

• Reproductive and • A number of • Some sediment • The VTG response may be • There is little difference Barucca et al. (2006),
endocrine parameters contaminants with contaminants induce used as a sensitive between the effects of Galloway et al. (2004),
(Physiological and widespread distribution in alterations in gonadal biomarker of exposure to different types of Martín-Díaz et al. (2004)
molecular) the environment are maturation of benthic estrogenic compounds and contaminants. and van der Oost et al.
reported to have endocrine organisms contaminants with known • All types of contaminants (2003)
activity, which might affect (measured through the affinity for the estrogenic have a serious inhibitory
reproduction and thus Gonadosomatic receptor such as effect on fish reproduction,
might threaten susceptible Index, GSI). nonylphenol, bisphenol A, even when in small
species. Hormone • The occurrence of PCBs, and PAHs. quantities, making
regulation may be protein vitellogenin/ determination of cause and
impaired as a consequence vitellin synthesis (VTG) in effect difficult.
of exposure to the blood of males and
contaminants. juveniles has been
considered largely a
specific biomarker for
hormone mimetic
contaminants in the
environment.
• Imposex (development of
male sexual characteristics
in female gastropods) and
intersex (any disturbance
of the congruity between
the gonad and genital
tracts) are also biomarkers
of endocrine disruption
resulting from xenobiotics.
• Stress proteins, • The stress proteins • Special groups of stress • The use of MT • Nutrition and external Galloway et al. (2004),
metallothioneins (MTs) (also called heat-shock proteins are the MTs or encompasses biochemical parameters such as pH, Martín-Díaz et al. (2004,
and multixenobiotic proteins, HSP) comprise a metallothionein-like responses from exposure temperature, salinity and 2007), Monserrat et al.
resistance set of abundant and proteins, which are a to metals (in particular Cu, dissolved oxygen can affect (2007) and van der Oost
(Molecular) inducible proteins involved family of low molecular Zn, Cd, and Hg). The the HSP response. et al. (2003)
in the protection and repair weight, cysteine-rich determination method is • Biological parameters
of the cell against stress proteins inducible by both well known and used, and such as age, biomass,
and harmful conditions. essential and non-essential does not require extensive health status and oxidative
metals and the resources or time for the stress may trigger the in-
P-glycoproteins of the analysis. duction process.
multixenobiotic resistance • MXR expression in • MT isoforms appear to be
(MXR) mechanism, which aquatic organisms such as differentially induced by
may be induced or bivalves, worms and various metals and affected
inhibited by a wide variety sponges, can be reliably by contamination
of chemicals. used as an indicator interactions.
of contaminant exposure • The biological function of
and/or resistance. MT is not fully understood.
It is, therefore, still not
possible to link changes in
MT levels to injury at the
cellular or organism level.
• Biotransformation • These biomarkers • Some PAHs are excreted • These biomarkers may • Most appropriate for fish. Galloway (2006), Galloway
products measure the elevation in as polar metabolites via the provide information on • Generally, the levels of et al. (2004) and van der
(Molecular) levels of biotransformation gallbladder (in bile), but both exposure and effects. bile metabolites are Oost et al. (2003)
products, such as most PAHs are excreted • Urine offers the indicative of short-term
metabolite levels in body after conjugation by phase advantage of requiring no exposure and therefore
fluids or the amount of II enzymes, thus the prior extraction due to the provide information on
covalent adducts formed biomarker more commonly physiological filtration recent exposure only.
between metabolites of used is PAH metabolites in afforded by the kidney,
biodegradable chemicals urine or bile. and is a nondestructive
and cellular biomarker.
macromolecules • Appropriate for
(proteins, RNA, DNA). PAH-contaminated sites.
• Biotransformation and • Enzymatic activity is an • The activities of these • The use of this battery of • Enzymatic activity Costa et al. (2009a),
antioxidant enzymes important indicator of enzymes may be induced biomarkers encompasses indicators are not always Martín-Díaz et al. (2004,
(Molecular) organism protection and or inhibited upon exposure biochemical responses associated with 2007), Monserrat et al.
reaction against to xenobiotics, according to from exposure to metals contaminants. Antioxidant (2007), Morales-Caselles
environmental stress. metabolizing phases I and organic compounds. enzymes are generally less et al. (2008, 2009),
Enzymes are involved in (reactions catalyzed by • Enzymes are one of the responsive to Valavanidis et al. (2006)
the detoxification of mixed-function more extensively contaminants than phase I and van der Oost et al.,
contaminants and their oxidase — MFO), II investigated biomarkers; and II enzymes. 2003)
metabolites (conjugation of the determination methods • Certain confounding
(biotransformation and contaminant parent are well known, and are variables may affect
antioxidant enzymes). compound or its not resource or time enzyme activities
• Oxygen toxicity is defined metabolites with an demanding. (e.g., EROD activity may
as injurious effects due to endogeneous ligand), or not only indicate chemical
cytotoxic reactive oxygen antioxidant enzymes. exposure but may also

(continued on next page)

82 P.M. Chapman et al. / Environment International 55 (2013) 71–91

Table 2 (continued)
Biomarker group Description Stressors triggering Appropriate use Disadvantages Reference
response

species (ROS) that can • Several enzymatic precede effects at various

induce deleterious effects
at the cellular level
(oxidative stress).
• Oxidative stress • Oxidant-mediated effects • Examples of these
parameters with potential suitability as biomarkers used in
(Molecular) biomarkers comprise
adaptive responses, such as lipid peroxidation (LPO);
increased activities of
antioxidant enzymes,
concentrations of
non-enzymatic
compounds, or
manifestations of
oxidant-mediated toxicity
such as oxidations of
proteins, lipids and nucleic TOSC is the capacity to
acids, as well as perturbed establish an integrated
tissue redox status.
• Neuromuscular • Neuromuscular functions • The biomarker
parameters can be affected by the
(Molecular) presence of contaminants
in the environment.
activities can be used;
those most common in
transitional water
sediment assessment
studies are: reduced
glutathione (GSH);
oxidized glutathione
(GSSG); glutathione
peroxidase (GPX);
glutathione transferase
(GT); glutathione
reductase (GR); mixed
function
oxidase-ethoxyresorufin–
O-deethylase (EROD);
dibenzylflourescein
dealkylase (DBF);
glutathione S-transferase
(GST); esterase activities;
induction of cytochrome
P450 1A (CYP1A); catalase
(CAT); superoxide
dismutase (SOD); and,
thiobarbitutic reactive
substances (TBARS).
• For example EROD,
CYP1A, GSH and GST are
implicated in the
detoxification of organic
trace compounds (e.g., PAH
and PCB) and GPX, CAT, GR
and SOD provide
protection of the organism
against oxidative stress.
transitional waters are:
and, the total oxyradical
scavenging capacity
(TOSC) assay. LPO is
composed of a set of chain
reactions, especially for
polyunsaturated fatty acids
which are sensitive to
oxidative reactions by ROS.
antioxidant response of an
organism or tissue against
a particular type of ROS.
• Total haemolymph
protein concentration, and
ferric reducing ability of
plasma (FRAP) can also be
used to measure
antioxidant activity.
acetylcholinesterase
(ACHE) is involved in the
deactivation of
acetylcholine at nerve
endings, preventing
continuous nerve firings,
which is vital for normal
functioning of sensory and
neuromuscular systems.
• ACHE is sensitive to
organophosphate (OP) and
carbamate pesticides and
may respond to low levels
of contaminants in the
environment.
• These biomarkers, in
particular LPO, provide
information on both
exposure and effects.
• Antioxidant defenses,
which are generally
ubiquitous in animal
species and different tissue
types, are found widely in
aquatic organisms.
• ACHE inhibition has been
used to assess the nature
and extent of exposure of
wildlife to agricultural and
forest sprays (using OP and
carbamate pesticides) that
reach the aquatic
environment. Since these
compounds have a
relatively short half-life,
the assessment of
cholinesterase inhibition is
a useful tool to evaluate
their potential impact on
aquatic biota, even when
the chemicals are no
longer detectable in the
environment.
levels of biological
organization).
•Many contaminants
(or their metabolites) may
elicit toxicity related to
oxidative stress, making it
difficult to determine cause
and effect.
• Dissolved oxygen and Costa et al. (2011b),
temperature are Galloway et al. (2004),
environmental variables Martín-Díaz et al. (2004),
that are likely to influence Monserrat et al. (2007),
oxidative processes. Valavanidis et al. (2006)
• LPO appears to have and van der Oost et al.
considerable potential as a (2003)
biomarker although it can
occur as a consequence of
cellular damage due to a
variety of insults other
than exposure to contami-
nants causing oxidative
stress.
• Many contaminants
(or their metabolites) may
elicit toxicity related to
oxidative stress, making it
difficult to establish cause
and effect.
• Complex mixtures of Monserrat et al. (2007) and
contaminants, other than van der Oost et al. (2003)
pesticides, could be
important sources of
ACHE-inhibiting
compounds in the aquatic
environment.
 P.M. Chapman et al. / Environment International 55 (2013) 71–91 83

Table 2 (continued)
Biomarker group Description Stressors triggering Appropriate use Disadvantages Reference
response

• Transcriptomics/ • Transcriptomics or
toxicogenomics toxicogenomics result from
(Molecular) the fusion between
conventional toxicology
and functional genomics,
based on advanced
molecular biology tools.
• Multiple endogenous and
exogenous variables
influence the
post-transcriptional
mechanisms that are
fundamental in the control
of gene expression.
• The most common tools
for these measurements
are cDNA microarrays,
oligonucleotide
microarrays, and serial
analysis gene expression.
Another technique is
expression analysis of
specific genes by reverse
transcription polymerase
chain reaction
(RT-PCR)-related
techniques, namely
real-time RT-PCR.
• Proteomic • Protein regulation pattern
(Molecular) or expression profile
change are responses to
stress conditions and often
indicate toxic exposure or
effect.
• Metabolomics • Metabolomics includes
(Molecular) the quantitative
measurement of
metabolism in response to
toxic or physiological
changes and is
complementary to
genomics and proteomic
approaches. Nuclear
Magnetic Resonance
(NMR) technology is
employed to complete the
information obtained by
the other two tools.
• Selected genes are usually
based on the potential
function of respective
proteins in response to
oxidative stress-related
biomarkers such as GPX,
CAT, MT, CYP1A, Heat
shock protein 90 kDa alpha
(HSP90AA), VTG and
Cysteine-aspartic acid
peptidase isoform 3
(CASP3).
• Deregulated proteins can
be related with
antioxidative cellular
defense processes, energy
production, proteolysis,
and contaminant
catabolism.
• The metabolomics
process involves the
capture of thousands of
signals for low molecular
weight metabolites in a
given matrix, followed by
use of statistical and data
reduction tools to
determine the sub-set of
signals that correlate with
the response measurement
(such as a disease state) in
the particular study design.
• These biomarkers provide • cDNA microarray Barucca et al. (2006), Costa
information on both technology application is et al. (2011c, 2012a) and
exposure and effects. costly and restricted to Martín-Díaz et al. (2004)
• Transcriptomics permit a taxa where considerable
screening of multiple genomic or expressed
responses, some of which sequence tag information is
have potential for available.
predictive environmental • Real-time RT-PCR can be
toxicology. applied to any species as
long as it is possible to
design primers from
consensus sequences to
directly survey the amount
of steady-state mRNA that
should reflect the
production and stability of
transcripts.
• These biomarkers provide • To characterize the Costa et al. (2012b) and
information on both proteome, only mass Martín-Díaz et al. (2004)
exposure and effects. spectrometry (MS) has the
• Proteomics can be sensitivity, selectivity and
employed to identify novel throughput to identify each
or unbiased biomarkers, protein. Limitations to
since it is clear that implementation of this
deregulation can be an technique are the small
indicator of stress on its peptide-mass fingerprint
own. database available and the
lack of relevant DNA
sequence information.
• In general all the “omics”
techniques are expensive
and require highly
experienced researchers
• These biomarkers provide • These are complicated Martín-Díaz et al. (2004)
information on both and expensive techniques and Sumner and Fennell
exposure and effects. associated with the (2007)
• These approaches can be complexities in
applied to higher levels of interpreting the
tiered toxicity metabolomics and
assessments. associated relationship to
xenobiotics.

and other stressors (Costa et al., 2011c, 2012a; Martín-Díaz et al.,
2004). A growing number of studies are determining changes in the
transcription regulation of specific genes in organisms related to
chemical stressors. While biomarkers of exposure such as MT are
based on the premise that exposure causes induction, chemical stress
can also cause down-regulation of some “omic” biomarker responses
during the early stages of stressor exposure as a result of general
metabolic impairment (Costa et al., 2012b). Transcriptomics and pro-
teomics are being used in transitional waters to link chemical contami-
nation with biological responses (Barucca et al., 2006; Costa et al.,
2011c, 2012b; Monserrat et al., 2007). Although the “omics” have great
potential (Gallagher et al., 2006), their utility in environmental studies,
particularly in transitional waters, is limited by our present lack of
understanding of the compartmentalization of metabolites across cells,
tissues, and biological fluids (Sumner and Fennell, 2007), and by the
complexity of mixture effects in contaminated sediments. In addition,
these techniques are expensive and their interpretation requires highly
experienced researchers. Future development and application of com-
puter models such as artificial neural networks may be helpful in deter-
mining relationships between “omics” and environmental stressors
(Bradley, 2012), but cannot establish causation.
Some biomarkers respond differently in the laboratory compared
to field conditions. These differences may be due to differences be-
tween controlled environmental variables (e.g., access to food,
dissolved oxygen, temperature, salinity, hydrodynamics) in the labo-
ratory compared to the field, which can affect not only organism
84
Table 3
Biomarkers of effects applied to transitional water environments.
Biomarker Description
group
• Morphological • Organism physiology and
and morphology are usually
histological assessed through
(Physiological) histopathological alterations
and gross morphological
indices.
• Determination of adverse
effects due to exposure to a
variety of anthropogenic
contaminants can be performed
histopathologically, by
investigating lesions,
alterations, or tumor formation
(neoplasms) in organism
tissues.
• These alterations are usually
assessed in liver, gills, kidneys,
gonads, and the digestive tract.
• Physiology • Growth as a process represents • The physiological energetic
(Physiological) an integration of major
physiological responses and
status and specifically the
balance between processes of
energy acquisition
(feeding and assimilation) and
energy expenditure
(metabolism and excretion).
• Physiological endpoints such
as heart rate alterations can
evaluate the general condition
of organisms exposed to
stressors.
• Immunological • A large number of
(Cellular) environmental chemicals have
the potential to impair
components of the immune
system, weakening host
immune defenses and making
them more susceptible to
epizootic infections. Both
antibody and cell mediated im- antigens and is the first line of
munity may be depressed by
certain contaminants.
• Hematological • Several hematological
(Cellular/ parameters are potential effect enzymes (e.g., transaminases)
molecular) biomarkers.
• Blood cells and their
organization are recognized as a membranes in certain organs.
convenient vector for analysis
since peripheral blood reflects
the global health status of the as hematocrit, hemoglobin,
individual.
P.M. Chapman et al. / Environment International 55 (2013) 71–91
Stressors triggering response Appropriate use Disadvantages Reference
• Histopathological alterations • Histopathological lesion • Resource and time demanding Chapman (1986),
are usually semi-quantitative assessment is robust, and requires prior knowledge of Costa
and evaluated by ranking the inexpensive and usually has normal/healthy and damaged et al. (2009b,
severity of lesions. good associations with tissues of each bioindicator 2011a, 2012a),
• Morphological parameters that contaminants in general. It is
species, thus a comparative Hinton et al.
are often determined as stressor particularly useful for approach is compulsory, as is (1992),
responses are the liver somatic contaminant mixtures, which the choice of an adequate Martín-Díaz et al.
index (LSI) to identify possible are commonly found in reference. Histopathological (2008b), Riba
liver diseases, and the condition transitional waters. traits differ from species to et al. (2004) and
factor (CF) to assess the general species. van der Oost et al.
condition of the organism based • LSI and CF parameters are not (2003)
on reaction patterns sensitive and may be affected by
(e.g., circulatory disturbance, non-contaminant factors (e.g.,
inflammatory response, season, disease, nutritional
regressive and progressive level); they may serve as an
alterations), and biological initial screening biomarker to
importance of the lesions. indicate exposure and effects or
to provide information on
energy reserves.
• There is a lack of specificity of
histopathological alterations to-
wards a given toxicant.
• These parameters are easy to • These parameters are Erk et al. (2011),
approach usually referred to as measure and inexpensive. non-specific in their responses Galloway et al.
Scope for Growth (SfG) is a • Decrease in CEA may result in a towards chemical stressors. (2004) and
general physiological response lower amount of energy avail- • They should never be used Hagger
to environmental stressors. A able for growth, reproduction, alone since transitional waters et al. (2009)
biochemical alternative to the or defense against stressors. represent a very demanding
physiological SfG can be cellular environment in terms of energy
energy allocation (CEA). CEA needed for maintenance of os-
quantifies available energy re- motic balance.
serves and energy consumption
at a cellular level of biological
organization and provides a net
cellular energy budget for the
organism.
• Heart rate is also a biomarker
that can be used to evaluate
physiological responses of
organisms exposed to environ-
mental stress.
• The immune system is • Although most research on • These parameters are Galloway et al.
extremely vulnerable to insult these parameters has been non-specific in their responses (2004),
from exogenous chemicals, performed on mammalian towards chemical stressors. Monserrat et al.
especially after chronic species, it is a promising field for • Other stresses, such as (2007), van der
exposure or repeated short new biomarkers in other handling, transportation or so- Oost et al. (2003)
exposures. The non-specific im- organisms. cial interactions among and Zelikoff et al.
mune system is non-dependent • Immune assays with fish have individuals and parasitism may (2002)
on previous exposure to foreign been employed successfully to cause immunological distur-
assess metal, pesticide, aromatic bances in organisms. In addi-
defense involved in inflamma- hydrocarbon, and mixture tion, three main categories of
tory response. induced immunotoxicity. hormones (i.e., corticoids,
• Many types of biomarkers have catecholamines, and opioid
been used; the most common peptides) have direct and
example in transitional waters indirect effects on various
is phagocytosis activity of aspects of the immune system.
haemocytes that measures
immunotoxicity or
lymphocyte proliferation.
• The leakage of specific • Hematological biomarkers • Only appropriate for organisms Costa et al.
reduce the need to sacrifice with blood that can readily be (2011b),
into the blood may be indicative organisms. removed. Galloway et al.
of the disruption of cellular • Blood samples can regularly be • Typically, hematological (2004),
obtained from test organisms. parameters are non-specific in Martín-Díaz et al.
Although less specific, other their responses towards chemi- (2004) and van
hematological parameters, such cal stressors. der Oost et al.
(2003)
protein, and glucose, may be
sensitive to certain types of
contaminants. In addition, the
blood levels of specific steroid
hormones or proteins normally
induced by these hormones may
be indicative of certain
 P.M. Chapman et al. / Environment International 55 (2013) 71–91 85

Table 3 (continued)
Biomarker Description Stressors triggering response Appropriate use Disadvantages Reference
group

reproductive effects due to

• Genotoxicity • The exposure of an organism to
(Molecular) genotoxic chemicals may induce
a sequence of events: formation
of structural alterations in DNA;
procession of DNA damage and
subsequent expression in
mutant gene products; and, dis-
eases (e.g., cancer) resulting
from altered function of
affected cells, which can lead to
uncontrolled cell proliferation.
There is an acknowledged link
between DNA damage and neo-
plasias. The consequence of
structural perturbations to the
DNA molecule, such as adducts
and secondary modifications,
may result in lesions that
become permanent.
endocrine disruption.
• Lysosomal integrity can also be
a hematological biomarker.
• The more common genotoxic
responses are: DNA strand
breaks that are produced,
either directly by the chemical
or its metabolite, or by the pro-
cessing of structural damage
(usually measured through the
Comet assay — the damage may
result from direct DNA chain
oxidation, formation of xenobi-
otic DNA adducts, and
alkali-labile sites);
DNA base composition;
oncogene activation;
cytogenetic effects
(e.g., erythrocitic nuclear
abnormalities ENA — usually
chromosomal clastogenesis);
and, tumorigenesis.
• The detection and • The techniques are time Costa and Costa
quantification of various events consuming if not using (2007, 2011b),
in this sequence may be automatic scorers Galloway et al.
employed as biomarkers of (as for the Comet assay). (2004),
exposure and effect in • Genotoxic assays such as Martín-Díaz et al.
organisms exposed to genotoxic the Comet assay require strict (2004),
substances in the environment. sampling measures, for instance Monserrat
• Organic contaminants such as animals must be captured alive et al. (2007),
PAHs, as well as metals and and analyses run immediately Shugart et al.
metalloids, although by after blood collection to assure (1992) and van
different means, all induce cell viability. der Oost
mutagenesis. • Requires a reference et al. (2003)
• The study of genetic toxicology comparison; technical
in aquatic systems is mainly inter-calibrations are neither
focused on carcinogenesis in reliable nor feasible.
fish and shellfish and is applied
to higher levels of tiered toxicity
assessments.

exposure but also contaminant bioavailability (Costa et al., 2011a,
2011b; Riba et al., 2005; van der Oost et al., 2003). The “bottom
line” is that laboratory biomarker measurements do not necessarily
predict how those biomarkers will respond under field conditions.
The following criteria can be used to determine the most useful
and appropriate biomarkers for environmental assessments (adapted
from: Martín-Díaz et al., 2004; van der Oost et al., 2003):
i. The assay to quantify any biomarker, including the biomarker
itself, should be reliable (with quality assurance), relatively
cheap, and easy to perform;
ii. The biomarker should respond to a stressor such as a chemical
contaminant in a dose-dependent manner;
iii. Biomarker response(s) should be sensitive to stressor exposure
and/or effects in order to serve as early warning parameters, in
other words they should have environmental relevance;
iv. The toxicological significance of any biomarker, i.e., the relation-
ships between its response and any (long term) effect to the or-
ganism, should be established;
v. The modifying effects of confounding factors to biomarker re-
sponses should be established (e.g., environmental factors,
non-specificity of the response);
vi. Biomarkers should be preferentially non-invasive and non-
destructive to allow or facilitate environmental monitoring
of stressor exposure and effects in protected or endangered
species;
vii. Biomarkers should be field validated;
viii. Biomarker responses should be consistent with one another;
and,
ix. Baseline biomarker data should be well defined in order to
distinguish between natural variability (stochastic noise)
and induced stress such as from a chemical contaminant
(signal).
As noted above (item v) and previously, modifying factors need to
be considered, in particular salinity in transitional waters (Erk et al.,
2011; Martín-Díaz et al., 2004; Pfeifer et al., 2005). Such modifying
factors need to be considered not only when choosing and deploying
biomarkers but also when interpreting the resulting data (van der
Oost et al., 2003). Other factors that should also be considered are:
morphological and physiological alterations and biota life-cycles
(Galloway et al., 2004; Liu et al., 2012; Monserrat et al., 2007); age
and size (Zielinski and Pörtner, 2000); season (Cravo et al., 2012;
Liu et al., 2012; Oliveira et al., 2009; Pfeifer et al., 2005; Serafim
et al., 2012); environmental parameters including pH, temperature
and dissolved oxygen (Costa et al., 2011b; Cravo et al., 2012; van
der Oost et al., 2003); nutrition (Costa et al., 2012a); and, length of
exposure (Amiard-Triquet, 2009) — longer exposures typically result
in more clear-cut responses (Costa et al., 2011c). Unfortunately, esti-
mates of all these confounding factor interactions are still scarce, as
evidenced by the extensive use of uncertainty factors in environmen-
tal risk assessment.
Responses established for one species are not necessarily valid for
other species. Also, presumably because of their relatively high sensitiv-
ity and complexity, biomarker responses can be difficult to interpret
(e.g., they are prone to false positives — Caeiro et al., 2012; van der
Oost et al., 2003). Thus, usually more than one biomarker is typically
employed in an integrative assessment, particularly where complex
mixtures of contaminants and other stressors are present as in transi-
tional waters (Costa et al., 2012a; Morales-Caselles et al., 2008, 2009).
Screening using multiple biomarkers can both supplement other LOE
and indicate biota and areas that require further investigation, trigger-
ing a cascade of biological responses (van der Oost et al., 2003). Com-
bining biomarkers of exposure and of effect at the molecular, cellular,
and whole organism level is recommended (Galloway et al., 2004; van
der Oost et al., 2003) — because there is no single biomarker that can
be used for all organisms and all stressors, and that provides informa-
tion on both exposure and effects.
Indices of biomarker responses can be developed based on statis-
tically significant differences between organisms exposed to contam-
inated and reference sediments (Benedetti et al., 2012; Costa et al.,
2012a; Hagger et al., 2009; Oliveira et al., 2009; Piva et al., 2011;
Serafim et al., 2012). One of the most widely used indices is the Inte-
grated Biomarker Response (IBR), originally proposed by Beliaeff and
Burgeot (2002). The indices can be computed with or without
weighting and with a threshold depending on the relevance of the
measured endpoint, species and tissues. However, the type and num-
ber of biomarkers used in any index needs to be selected cautiously.
Further, such indices only allow a qualitative assessment, must be
carefully interpreted, and cannot serve as the only LOE for manage-
ment decision-making.
86 P.M. Chapman et al. / Environment International 55 (2013) 71–91
The most immediately useful LOEs to combine with biomarkers
are chemical analyses both of external concentrations and internal
doses, and bioindicator responses from toxicity tests (Martín-Díaz
et al., 2004; Morales-Caselles et al., 2009; van der Oost et al., 2003).
Field validation (i.e., the resident biota LOE) is more useful in terms of
the “big picture” because, due to stochasticity, it will not be as discrimina-
tory as the other two LOEs combined with biomarker responses (i.e., early
warning or even low level effects may go undetected due to natural
variability).
5.1. Summary
Biomarkers are a promising, powerful, and improving LOE
(Galloway, 2006) that can be measured for organisms subjected to
toxicity testing under controlled laboratory conditions and/or in situ
in the field. They can be useful in terms of both screening and
assisting in determining causation for sediments in geochemically
complex transitional waters (Benedetti et al., 2012; Costa et al.,
2011b, 2012a; Cravo et al., 2012; Picado et al., 2007). The biomarker
LOE should include both biomarkers of exposure and of effects since
one cannot necessarily predict the other, and should involve testing
more than one species. Guidance regarding the applicability of differ-
ent biomarkers to transitional waters is provided.
6. Integrative assessments
6.1. Different approaches to integration
Integration of different LOEs to provide the best information for
informed decision-making is essential given the natural complexity
of transitional waters (physical, biological, and chemical stressors)
coupled with mixtures of chemical contaminants found in their sedi-
ments (additional chemical stressors) and the reality of climate
change (influencing all currently existing stressors). For example, al-
though univariate and multivariate analyses of benthic community
structure can detect alterations when stressor influences are strong,
the addition of toxicity testing is necessary to detect effects of subtle
stressor influences (Rubal et al., 2009). Such integration is typically
accomplished using a WOE approach.
WOE as a concept is well accepted among scientists and managers. It
includes various quantitative approaches including univariate and mul-
tivariate analyses (Burton et al., 2002a; Dafforn et al., 2012; Linkov et al.,
2009; Suter and Cormier, 2011; Weed, 2005) and can include meta-
analysis (Hedges and Olkin, 1985; Kapo et al., 2008) and multi-criteria
decision analyses (Sparrevik et al., 2012). Bayesian approaches, which
are particularly useful when data are sparse, are gaining in importance
for both determining probabilities of ecosystem status (e.g., that a cer-
tain status is the desired status) and decision-making in the face of un-
certainty (Barton et al., 2012).
WOE is a form of synthesis, as recommended for estuaries and
other transitional waters (Kemp and Boynton, 2012) and can incor-
porate relative risk modeling (Chen et al., 2012). It is defined as
(Burton et al., 2002b) “a process used… to evaluate multiple lines-
of-evidence concerning ecological condition”. Presently, in the ab-
sence of mechanistic stressor-response linkages, WOE relies more
on best professional judgment (BPJ — cf. Burton et al. (2002b) and
Chapman and Anderson (2005) for more information regarding the
use of BPJ within sediment quality assessments) than on statically-
based decision points; hence, transparency in the use of WOE is crit-
ically important. Transparency is particularly important regarding both
the weight given to particular LOE and specific integration methodology,
both of which require a relatively high degree of site- and situation-
specific flexibility. As Linkov et al. (2011) note in recommending use
of multicriteria decision analyses as part of any WOE assessment:
“Each WOE method is based on a unique rationale and capable of
considering a different scope of LOEs. Thus, each method has specific
benefits and drawbacks. The different nature of methods means that
one cannot a priori determine the superior method for a particular
application. One must consider the method employed in addition
to the evidence.”
Bay and Weisberg (2012) provide a framework for assessing labo-
ratory toxicity data independently against sediment chemistry and
benthic infaunal community data to determine, respectively, the po-
tential for a chemically mediated effect and the severity of effect. Po-
tential and severity are then combined to determine whether a site is:
unimpacted; likely unimpacted; possibly impacted; likely impacted;
clearly impacted; or, inconclusive. Greatest weight is given to the
benthic infaunal data; chemistry and toxicity data are given a lower
weight. These authors do not consider biomarker data or how they
might fit into this framework; however, such integration is consid-
ered by other authors (Davies and Vethaak, 2012; Lyons et al., 2010;
Thain et al., 2008). As previously noted, we suggest that biomarkers
be measured in organisms subjected to laboratory toxicity testing
and/or in the field, and that these data be used for screening and
assisting in determining causation.
6.2. Dealing with uncertainty
What is measured in the laboratory and what actually occurs in
the field can be very different (Hose et al., 2006). For example, pop-
ulations of the ragworm polychaete, Nereis diversicolor, survive and
apparently thrive in the highly metal-contaminated upper reaches
of Restronguet Creek (Cornwall, UK) despite free spawning their
sperm onto sediments containing concentrations of copper and
cadmium that should kill those sperm (Lewis and Ford, 2012). As
noted previously, laboratory biomarker measurements do not nec-
essarily predict how those biomarkers will respond under field
conditions. Tolerance to metal contaminants such as copper can
vary between populations of the same species (Burlinson and
Lawrence, 2007). Organisms living in metal-contaminated sedi-
ments may accumulate more metal than laboratory test organisms
exposed to those sediments (Schlekat et al., 2000). Rosen et al.
(2012) emphasize the need to include in situ studies as the results
from laboratory studies do not necessarily explain effects that may
be observed in the field (e.g., groundwater seepage effects are not
considered).
As previously noted, WOE depends on a certain level of BPJ, which is
itself a source of uncertainty (i.e., agreement or lack of such between
experts — Batley et al., 2002; Bay et al., 2007; Thompson et al., 2012).
Uncertainty related to the use of BPJ will be less important at the ex-
tremes (e.g., sites that are clearly contaminated and toxic, and those
that are clearly not) than between the extremes. Steps to reduce uncer-
tainty in WOE assessments are suggested below — based on our modi-
fications and additions to recommendations originally provided by Bay
et al. (2007):
1. A priori agreement on: specific LOE to be used; components of
those LOE; and, methodologies for measuring, assessing and
reporting each LOE. The LOE should adequately characterize all
conditions and stressors (physical, chemical and biological).
2. A priori determination of and agreement on key elements of the
WOE assessment strategy including, but not restricted to: relative
weight of each LOE; how multiple LOE will be combined; and,
how conclusions will be determined. Per Weed (2005) a solid the-
oretical foundation should be established to integrate different
LOEs, not an arbitrary weighting scheme. Although weighting of
LOE cannot be generalized due to site- and situation-specific dif-
ferences, clearly LOEs that are linked to assessment endpoints
that comprise communities, populations, or ecosystem services
(see Section 7, Management and Decision-Making) should have
greater weight than those that are not so linked.
 P.M. Chapman et al. / Environment International 55 (2013) 71–91
3. A posteriori review of interpretation of individual LOE and overall
WOE by qualified individuals involved in steps 1 and 2, above, but
who were not involved further in the mechanics of data collection,
analyses, assessment and integration — effectively a check on both
technical defensibility and sensibility of the determinations. This
review needs to ensure that WOE assessments are “flexible, trans-
parent and defensible… and generate creative solutions to difficult
problems” (Suter and Cormier, 2011).
6.3. Establishing causation
Establishing causation requires knowledge of all stressors, recep-
tors, and potential activities that could affect both in any transitional
water body and adjoining terrestrial environments. For example,
bottom-trawling can be a major source of contaminant release from
sediments and uptake by aquatic organisms (Bradshaw et al., 2012).
Diffuse landscape-scale risks (e.g., weeds, feral pigs, fires) can be sev-
eral orders of magnitude greater than risks from contaminants
(Bayliss et al., 2012).
USEPA (U.S. Environmental Protection Agency) (2010) has
established the Causal Analysis/Diagnosis Decision Information Sys-
tem (CADDIS). Newman et al. (2007) provide guidance for formally
identifying the most plausible stressor(s) in complex coastal systems
and recommend that Bayesian analyses be used to develop questions
and hypotheses focused on causal relationships for LOE and WOE.
Anderson et al. (2010) provide an example of a sediment toxicity
evaluation procedure for identifying sediment contaminants associated
with laboratory toxicity.
6.4. Summary
Integrative WOE assessments should allocate the greatest weight to
benthic infaunal data; chemistry and toxicity data have lower weight.
The biomarker LOE should be assessed together with the sediment
chemistry and laboratory toxicity LOE. Guidance is provided regarding:
different approaches to integration; dealing with uncertainty; and,
establishing causation.
7. Management and decision-making
Adaptive management is particularly required for sediments in
transitional water bodies — an evidence-based learning process
“based on reducing uncertainties, considering possibilities and calcu-
lating risks” (Laane et al., 2012). Such management needs to consider
all possible interactions between stressors and receptors; for in-
stance, the possibility that transitional waters pose a toxic contamina-
tion risk to wading birds (Smith et al., 2009). Management actions for
contaminated aquatic sediments are outlined in Chapman and Smith
(2012) including post-remedial monitoring and are not repeated
herein. Here we emphasize the importance of ecosystem services in
management and decision-making for contaminated sediments in
transitional water bodies in the larger context of the overall aquatic
ecosystem. But we also caution that, as exampled by Lemming et al.
(2012) management options need to be carefully evaluated including
life cycle analyses, as they too often “result in higher environmental
impacts than they remediate”.
7.1. Ecosystem services
The overall goal of environmental management has generally been
to protect populations and communities, not individuals — with the ex-
ception of endangered or charismatic species (Suter et al., 2005).
Attempts to protect individual species are misguided given natural
stochasticity, population resilience, and “approved” human stressors
such as fishing. Arguably, we are at the point of going further to protect
ecosystem services, in other words the value of the environment
87
to human well-being, particularly high-value coastal ecosystems
(Costanza et al., 1997). Specifically, we need to begin ignoring changes
to non-human, non-charismatic populations and communities provided
ecosystem services are maintained.
Transitional water bodies provide ecosystem services that include:
provision of food for humans both directly and indirectly via their
high biological productivity and nutrient cycling; sites for recreation;
disease regulation (e.g., salt water inhibiting mosquito larvae); water
purification and waste treatment (e.g., contaminant removal from
inflowing waters to sediments); and, locations conducive to human set-
tlement and development (e.g., urban, port, and industrial activities).
They are high-value ecosystems, with potentially conflicting uses of
their ecosystem services. Ecosystem services provided by sediments
are detailed in Wall (2004).
Protection of ecosystem services increases the relevance of
environmental assessments by focusing on why changes in current
populations/communities matter (or not) to humans (Fisher et al.,
2009) but requires integrating those services with societal benefits
(Atkins et al., 2011). Because ecosystem services are not restricted
to transitional waters but also extend to adjoining terrestrial and ma-
rine areas (e.g., sources of agricultural run-off, habitat loss from con-
struction, effluent discharge), their consideration as the ultimate
end-point for management decision-making allows for assessment
of trade-offs where optimizing delivery of a given service (e.g., agricul-
ture) may impair another (e.g., commercial fish species in transitional wa-
ters) (Chapman, 2012). River diversions for flood control and wetland
restoration provide another example of trade-offs, in this case human
needs and wants versus resulting shifts in community composition (Das
et al., 2012).
7.2. Management of ecosystem services in transitional water bodies
There are four types of ecosystem services (MEA, Millennium
Ecosystem Assessment, 2003), all of which apply to and need to be man-
aged in transitional water bodies (O'Higgins et al., 2010): provisioning,
including food, fiber, and freshwater; regulating, including climate and
air-quality; cultural, including spiritual, religious, esthetic, and educa-
tional; and, supporting, including nutrient cycling, photosynthesis, and
refugia functions. Ecosystem services can in some cases be readily mea-
sured in terms of a monetary value (e.g., commercial fisheries) and in
other cases monetary values are variable and subject to much uncer-
tainty (e.g., maintenance of water quality).
Menzie et al. (2012) argue that valuation of ecosystem services
needs to be holistic, based on knowledge of ecosystem dynamics,
and that a reductionist approach will undervalue the services that
ecosystems provide and which will vary both seasonally and over
longer time periods — particularly for transitional water bodies.
Pascual et al. (2012) provide an example of sewage treatment con-
tributing to an improvement in an estuary's environmental and bio-
logical features, and to an increase in the ecosystem services
provided — but the environmental effects of treatment other than
monetary costs were not considered. Management of ecosystem ser-
vices must consider all direct and indirect effects of any management
actions both within transitional waters and for associated terrestrial
environments. For example, natural processes can, if allowed to oper-
ate, provide restoration through recolonization (Griffiths et al., 2011).
Full restoration from extensive degradation can take decades (Borja
et al., 2010); however, restoration from dredging can occur in about
1 year (Ceia et al., 2013).
Management of ecosystem services must be adaptive embodying
six key principles (as modified from NRC, 2004): clearly define the
ecosystem services and their inter-relationships; develop conceptu-
al models based on these services that include both geographic and
temporal components (i.e., consider both space and time); formulate
management questions as testable hypotheses; test these hypothe-
ses to provide future management guidance; conduct appropriate
88 P.M. Chapman et al. / Environment International 55 (2013) 71–91
ongoing monitoring and assessment; and, revise management ac-
tions with new cycles of learning. These six key principles are consis-
tent with the sediment assessment and management framework
proposed by Chapman and Smith (2012), which as noted previously
includes monitoring and assessment of any remedial actions — a
principle that is unfortunately rare in most sediment assessment
frameworks or management actions. The importance of determining
whether actions had their intended consequences cannot be
overemphasized, particularly given the reality of climate change
and consequent overarching changes to transitional waters and as-
sociated ecosystems.
7.3. Summary
Ecosystem services provided by aquatic sediments as a component
of transitional waters need to be adaptively managed. Management ac-
tions for contaminated aquatic sediments including post-remedial
monitoring (Chapman and Smith, 2012) need to be undertaken where
necessary and appropriate following the six key principles explained
above (NRC, 2004).
8. Concluding remarks
Science needs to inform policy and test policy decisions. Specifically,
we need to, as highlighted by Polasky et al. (2011) “consider not only
the future impacts of current decisions, but also the potential for learn-
ing from decisions that can help inform future decisions.” Each of the
above sections concludes with a Summary of the guidance provided
for assessment and management of transitional waters relative to that
advice.
Sediment management in transitional waters needs to be sustain-
able, including hydrodynamic and other processes at local and larger
scales (Apitz, 2011), using different LOEs appropriately and incorpo-
rating them into integrative assessments for management decision-
making as discussed previously. Although scientific knowledge has
improved and will continue to improve, management decisions, par-
ticularly in transitional waters, must still be made without complete
information and will require triage, a word derived from the French
work trier which means ‘to sort’, in other words a process of prioriti-
zation based upon clear goals and allocation of resources (Bottrill
et al., 2008), hence the importance of screening and integrative as-
sessments based on WOE.
Trade-offs between environmental, socio-political and economic
impacts including stakeholder values can and should be assessed in
transitional waters by multi-criteria decision analysis (MCDA; Huang
et al., 2011) and/or decision theory (Polasky et al., 2011). In this context,
ecosystem services in transitional waters need to be valued not solely in
monetary terms, but considering (Abson and Termansen, 2010)
“trade-offs between the current flow of benefits from ecosystems and
the ability of those ecosystems to provide future flows.”
Humans have historically affected the ecology of transitional wa-
ters, either unintentionally (e.g., productivity in New Bedford Harbor,
MA, USA was benthic-dominated when European colonists first ar-
rived but changed to pelagic-dominated [Chmura et al., 2004]) or in-
tentionally by restricting coastal processes (e.g., Chapman, 2012). We
need to begin intentional interventions where necessary and appro-
priate to maintain essential ecosystem services associated with sedi-
ments in transitional water bodies.
Acknowledgments
We thank two anonymous referees for their useful comments,
which improved the manuscript.
References
Abson DJ, Termansen M. Valuing ecosystem services in terms of ecological risks and
returns. Conserv Biol 2010;25:250–8.
Amiard-Triquet C. Behavioral disturbances: the missing link between sub-organismal
and supra-organismal responses to stress? Prospects based on aquatic research.
Human Ecol Risk Assess 2009;15:87-110.
Anderson BS, Lowe S, Phillips BM, Hunt JW, Vorhees J, Clark S, et al. Relative sensitivi-
ties of toxicity test protocols with the amphipods Euhaustorius estuarius and
Ampelisca abdita. Ecotoxicol Environ Saf 2008;69:24–31.
Anderson BS, Phillips BM, Hunt JW, Clark SL, Voorhees JP, Tjeerdema RS, et al. Evaluation of
methods to determine causes of sediment toxicity in San Diego Bay, California, USA.
Ecotoxicol Environ Saf 2010;73:534–40.
Apitz S. Sustainable sediment management? Integr Environ Assess Manag 2011;7:691–3.
Atkins JP, Burdon D, Elliott M, Gregory AJ. Management of the marine environment:
integrating ecosystem services and societal benefits with the DPSIR framework
in a systems approach. Mar Pollut Bull 2011;62:215–26.
Banks J, Ross DJ, Keough MJ. Short-term (24 h) effects of mild and severe hypoxia (20%
and 5% dissolved oxygen) on metal partitioning in highly contaminated estuarine
sediments. Estuar Coast Shelf Sci 2012a;99:121–31.
Banks J, Ross DJ, Keough MJ, Eyre BD, Macleod CK. Measuring hypoxia induced metal
release from highly contaminated estuarine sediments during a 40 day laboratory
incubation experiment. Sci Total Environ 2012b;420:229–37.
Barbone E, Rosati I, Reizopoulou S, Basset A. Linking classification boundaries to
sources of natural variability in transitional waters: a case study of benthic
macroinvertebrates. Ecol Indic 2012;12:105–22.
Barton DN, Kuikka S, Varis O, Uusitalo L, Henriksen HJ, Borsuk M, et al. Bayesian net-
works in environmental and resource management. Integr Environ Assess Manage
2012;8:418–29.
Barucca M, Canapa A, Olmo E, Regoli F. Analysis of vitellogenin gene induction as a
valuable biomarker of estrogenic exposure in various Mediterranean fish species.
Environ Res 2006;101:68–73.
Batley GE, Burton Jr GA, Chapman PM, Forbes VE. Uncertainties in sediment quality
weight of evidence (WOE) assessments. Human Ecol Risk Assess 2002;8:
1517–47.
Bay SM, Weisberg SB. Framework for interpreting sediment quality triad data. Integr
Environ Assess Manage 2012;8:589–96. [erratum p 773].
Bay S, Berry W, Chapman PM, Fairey R, Gries T, Long E, et al. Evaluating consistency of
best professional judgment in the application of a multiple lines of evidence sedi-
ment quality triad. Integr Environ Assess Manage 2007;3:491–7.
Bay SM, Ritte KJ, Vidal-Dorsch DE, Field LJ. Comparison of national and regional sedi-
ment quality guidelines for classifying sediment toxicity in California. Integr Envi-
ron Assess Manage 2012;8:597–609.
Bayliss P, van Dam RA, Bartolo RE. Quantitative ecological risk assessment of the
Magela Creek Flooplain in Kakadu National Park, Australia: comparing point source
risks from the Ranger Uranium Mine to diffuse landscape-scale risks. Human Ecol
Risk Assess 2012;18:115–51.
Beliaeff T, Burgeot T. Integrated biomarker response: a useful tool for ecological risk as-
sessment. Environ Toxicol Chem 2002;21:1316–22.
Benedetti M, Ciaprini F, Piva F, Onorati F, Fattorini D, Notti A, et al. A multidisciplinary
weight of evidence approach for classifying polluted sediments: integrating sedi-
ment chemistry, bioavailability, biomarkers responses and bioassays. Environ In-
tern 2012;38:17–28.
Benjamin JR, Baxter CV. Is a trout a trout? A range-wide comparison shows nonnative
brook trout exhibit greater density, biomass, and production than native inland
cutthroat trout. Biol Invas 2012;14:1865–79.
Bianchi TS. Biogeochemistry of estuaries. Oxford, UK: Oxford University Press; 2007.
Borja A, Dauer DM, Elliott M, Simenstad CA. Medium- and long-term recovery of estu-
arine and coastal ecosystems: patterns, rates and restoration effectiveness. Estuar
Coasts 2010;33:1249–60.
Bottrill MC, Joseph LN, Carwardine J, Bode M, Cook C, Game ET, et al. Is conservation
triage just smart decision making? TREE 2008;23:649–54.
Boudreau BP, Jorgensen BB. The benthic boundary layer: transport processes and bio-
geochemistry. New York, NY, USA: Oxford University Press; 2001.
Bradley BP. Finding biomarkers is getting easier. Ecotoxicology 2012;21:631–6.
Bradshaw C, Tjensvoll I, Sköld M, Allan IJ, Molvaer J, Magnusson J, et al. Bottom trawling
resuspends sediments and releases bioavailable contaminants in a polluted fjord.
Environ Pollut 2012;170:232–41.
Burlinson FC, Lawrence AJ. A comparison of acute and chronic toxicity tests used
to examine the temporal stability of a gradient in copper tolerance of Hediste
diversicolor from the Fal estuary, Cornwall, UK. Mar Pollut Bull 2007;54:
66–71.
Burton Jr GA, Chapman PM, Smith ES. Weight-of-evidence approaches for assessing
ecosystem impairment. Human Ecol Risk Assess 2002a;8:1657–73.
Burton Jr GA, Batley GE, Chapman PM, Forbes VE, Smith EP, Reynoldson T, et al. A
weight-of-evidence framework for assessing sediment (or other) contamination:
improving certainty in the decision-making process. Human Ecol Risk Assess
2002b;8:1675–96.
Byrne PA, O'Halloran J. The role of bivalve mollusks as tools in estuarine sediment
toxicity testing: a review. Hydrobiologia 2001;465:209–17.
Caeiro S, Chapman PM, Delvalls A. Considerations for integrative environmental assess-
ments of contaminated estuarine sediments. Manage Environ Qual 2012;23:
400–13.
Campana O, Simpson SL, Spadaro DA, Blasco J. Sub-lethal effects of copper to benthic
invertebrates explained by sediment properties and dietary exposure. Environ
Sci Technol 2012;46:6835–42.
 P.M. Chapman et al. / Environment International 55 (2013) 71–91
Carreira S, Costa PM, Martins M, Lobo J, Costa MH, Caeiro S. Surveying ecotoxicological
heterogeneity in estuarine habitats through the integration of biomarkers and sed-
iment contamination profiles: a case study with a commercial clam. Arch Environ
Contam Toxicol 2013;64:97-109.
Castro H, Ramalheira F, Quintino V, Rodrigues AM. Amphipod acute and chronic sedi-
ment toxicity assessment in estuarine environmental monitoring: an example
from Ria de Aveiro, NW Portugal. Mar Pollut Bull 2006;53:91–9.
Ceia FR, Patrício J, Franco J, Pinto R, Fernández-Boo S, Losi V, et al. Assessment of estu-
arine macrobenthic assemblages and ecological quality status at a dredging site in
Southern Europe estuary. Ocean Coastal Manage 2013;72:80–92.
Chapman PM. Measurements of the short-term stability of interstitial salinities in
subtidal estuarine sediments. Estuar Coast Shelf Sci 1981;12:67–81.
Chapman PM. Sediment quality criteria from the sediment quality triad: an example.
Environ Toxicol Chem 1986;5:957–64.
Chapman PM. Presentation and interpretation of Sediment Quality Triad data. Ecotoxicology
1996;5:327–39.
Chapman PM. Determining when contamination is pollution — weight of evidence de-
terminations for sediments and effluents. Environ Intern 2007;33:492–501.
Chapman PM. Management of coastal lagoons under climate change. Estuar Coast Shelf
Sci 2012;110:32–5.
Chapman PM, Anderson J. A decision-making framework for sediment contamination.
Integr Environ Assess Manage 2005;1:163–73.
Chapman PM, Brinkhurst RO. Seasonal changes in interstitial salinities and seasonal
movements of subtidal benthic invertebrates in the Fraser River estuary, BC. Estuar
Coast Shelf Sci 1981;12:49–66.
Chapman PM, Hollert H. Should the Sediment Quality Triad become a tetrad, a pentad,
or possibly even a hexad? J Soil Sed 2006;6:4–8.
Chapman PM, Smith M. Assessing, managing and monitoring contaminated aquatic
sediments. Mar Pollut Bull 2012;64:2000–4.
Chapman PM, Wang F. Assessing sediment contamination in estuaries. Environ Toxicol
Chem 2001;20:3-22.
Chapman PM, Wang F, Adams W, Green A. Appropriate applications of sediment quality
values for metals and metalloids. Environ Sci Technol 1999;33:3937–41.
Chen Q, Liu J, Ho KC, Yang Z. Development of a relative risk model for evaluating eco-
logical risk of water environment in the Haihe River Basin estuary area. Sci Total
Environ 2012;420:79–89.
Chmura GL, Santos A, Pospelova V, Spasojevic Z, Ram R, Latimer JS. Response of three
paleo-primary production proxy measures to development of an urban estuary.
Sci Total Environ 2004;320:225–43.
Cobelo-Garcia A, Turner A, Millward GE. Fractionation and reactivity of platinum group
elements during estuarine mixing. Environ Sci Technol 2008;42:1096–101.
Costa PM, Costa MH. Genotoxicity assessment in fish peripheral blood: a method for a
more efficient analysis of micronuclei. J Fish Biol 2007;71:148–51.
Costa FO, Neuparth T, Correia AD, Costa MH. Multi-level assessment of chronic toxicity
of estuarine sediments with the amphipod Gammarus locusta: II. Organism and
population-level endpoints. Mar Environ Res 2005;60:93-110.
Costa PM, Caeiro S, Diniz M, Lobo J, Martins M, Ferreira AM, et al. Biochemical end-
points on juvenile Solea senegalensis exposed to estuarine sediments: the effects
of contaminant mixtures on metallothionein and CYP1A induction. Ecotoxicology
2009a;18:988-1000.
Costa PM, Diniz MS, Caeiro S, Lobo J, Martins M, Ferreira AM, et al. Histological bio-
markers in liver and gills of juvenile Solea senegalensis exposed to contaminated
estuarine sediments: a weighted indices approach. Aquat Toxicol 2009b;92:
202–12.
Costa PM, Caeiro S, Lobo J, Martins M, Ferreira AF, Caetano M, et al. Estuarine ecological
risk based on hepatic histopathological indices from laboratory and in situ tested
fish. Mar Pollut Bull 2011a;62:55–65.
Costa PM, Neuparth TS, Caeiro S, Lobo J, Martins M, Caetano M, et al. Assessment of the
genotoxic potential of contaminated estuarine sediments in fish peripheral blood:
laboratory versus in situ studies. Environ Res 2011b;111:25–36.
Costa PM, Miguel C, Caeiro S, Lobo J, Martins M, Ferreira AM, et al. Transcriptomic anal-
yses in a benthic fish exposed to contaminated estuarine sediments through labo-
ratory and in situ bioassays. Ecotoxicology 2011c;20:1749–64.
Costa PM, Caeiro S, Vale C, DelValls TA, Costa MH. Can the integration of multiple bio-
markers with sediment geochemistry solve the complexity of sediment risk assess-
ment? A case study with a benthic fish. Environ Pollut 2012a;161:107–20.
Costa PM, Chicano-Gálvez E, Caeiro S, Lobo J, Martins M, Ferreira AM, et al. Hepatic
proteome changes in Solea senegalensis exposed to contaminated estuarine
sediments: a laboratory and in situ survey. Ecotoxicology 2012b;21:1194–207.
Costa PM, Carreira S, Costa MH, Caeiro S. Development of histopathological indices in a
commercial marine bivalve (Ruditapes decussatus) to determine environmental
quality. Aquat Toxicol 2013;126:442–54.
Costanza R, d'Arge R, de Groot R, Farberk S, Grasso M, Hannon B, et al. The value of the
world's ecosystem services and natural capital. Nature 1997;387:253–60.
Cravo A, Pereira C, Gomes T, Cardoso C, Serafim A, Almeida C, et al. A
multibiomarker approach in the clam Ruditapes decussatus to assess the impact
of pollution in the Ria Formosa lagoon, South Coast of Portugal. Mar Environ
Res 2012;75:23–34.
Cripe GM. Contaminated sediment testing with the bivalve Mulinia lateralis: culture
refinement for organism availability. Environ Toxicol Chem 2006;25:1332–6.
Dafforn KA, Simpson SL, Kelaher BP, Clark GF, Komyakova V, Wong CKC, et al. The chal-
lenge of choosing environmental indicators of anthropogenic impacts in estuaries.
Environ Pollut 2012;163:207–17.
Das A, Justic D, Inoue M, Hoda A, Huang H, Park D. Impacts of Mississippi River diver-
sions on salinity gradients in a deltaic Louisiana estuary: ecological and manage-
ment implications. Estuar Coastal Shelf Sci 2012;111:17–26.
89
Dauvin J-C, Ruellet T. The estuarine quality paradox: is it possible to define an ecological
quality status for specific modified and naturally stressed estuarine ecosystems?
Mar Pollut Bull 2009;59:38–47.
Davies IM, Vethaak AD. Integrated marine environmental monitoring of chemicals and
their effects. ICES (International Council for the Exploration of the Sea) cooperative
research report no. 315; 2012 [http://www.ices.dk/products/cooperative.asp (Accessed
February 5, 2013)].
De Backer A, Van Coillie F, Montserrat F, Provoost P, Van Colen C, Vincx M, et al. Bioturba-
tion effects of Corophium volutator: importance of density and behavioural activity.
Estuar Coastal Shelf Sci 2011;91:306–13.
Dissanayake A, Galloway TS, Jones MB. Seasonal differences in the physiology of
Carcinus maenas (Crustacea: Decapoda) from estuaries with varying levels of an-
thropogenic contamination. Estuar Coastal Shelf Sci 2011;93:320–7.
Elliott M, Quintino V. The Estuarine Quality Paradox, environmental homeostasis and
the difficulty of detecting anthropogenic stress in naturally stressed areas. Mar
Pollut Bull 2007;54:640–5.
Environment Canada Ontario Ministry of the Environment. Canada–Ontario decision-
making framework for assessment of Great Lakes contaminated sediment. Ottawa,
ON, Canada; 2008.
Erk M, Ivankovic D, Strizak Z. Cellular energy allocation in mussels (Mytilus
galloprovincialis) from the stratified estuary as a physiological biomarker. Mar Pollut
Bull 2011;62:1124–9.
European Communities. Directive 2000/60/EC of the European Parliament and of the
Council of 23 October 2000 establishing a framework for community action in
the field of water policy. Off J European Comm 2000;43(L327). [75 pp.].
Ferraro SP, Cole FA. Ecological periodic tables for benthic macrofaunal usage of estua-
rine habitats: insights from a case study in Tillamook Bay, Oregon, USA. Estuar
Coast Shelf Sci 2012;102–103:70–83.
Fisher DJ, McGee BL, Wright DA, Yonkos LT, Ziegler GP, Turley SD. The effects of sieving
and spatial variability of estuarine sediment toxicity samples on sediment chemis-
try. Arch Environ Contam Toxicol 2004;47:448–55.
Fisher B, Turner R, Morling P. Defining and classifying ecosystem services for decision
making. Ecol Econ 2009;68:643–53.
Frenzilli G, Nigro M, Lyons BP. The Comet assay for the evaluation of genotoxic impact
in aquatic environments. Mutat Res 2009;681:80–92.
Gale SA, King CK, Hyne RV. Chronic sublethal sediment toxicity testing using the estu-
arine amphipod, Melita plumulosa (Zeidler): evaluation using metal-spiked and
field-contaminated sediments. Environ Toxicol Chem 2006;25:1887–98.
Gallagher K, Benson W, Brody M, Fairbrother A, Hasan J, Klaper R, et al. Genomics:
applications, challenges, and opportunities for the U.S. Environmental Protection
Agency. Human Ecol Risk Assess 2006;12:572–90.
Galloway TS. Biomarkers in environmental and human health risk assessment. Mar
Pollut Bull 2006;53:606–13.
Galloway TS, Brown RJ, Browne MA, Dissanayake A, Lowe D, Jones MB, et al. Multibiomarker
approach to environmental assessment. Environ Sci Technol 2004;38:1723–31.
Gamito R, Pasquaud S, Courrat A, Drouineau H, Fonseca VF, Conçalves C, et al. Influence
of sampling effort on metrics of fish-based indices for the assessment of estuarine
ecological quality. Ecol Ind 2012;23:9-18.
Gomiero A, Dagnino A, Nasci C, Viarengo A. The use of protozoa in ecotoxicology: ap-
plication of multiple endpoint tests of the ciliate E. crassus for the evaluation of
sediment quality in coastal marine ecosystems. Sci Total Environ 2013;442:
534–44.
Greenstein DJ, Bay SM. Selection of methods for assessing sediment toxicity in Califor-
nia bays and estuaries. Integr Environ Assess Manage 2012;8:625–37.
Griffiths AM, Ellis JS, Clifton-Dey D, Machado-Schiaffino G, Bright D, Garcia-Vazquez E, et al.
Restoration versus recolonization: the origin of Atlantic salmon (Salmo salar L.) currently
in the River Thames. Biol Conserv 2011;144:2733–8.
Hack LA, Tremblay LA, Wratten SD, Forrester G, Keesing V. Toxicity of estuarine sedi-
ments using a full life-cycle bioassay with the marine copepod Robertsonia
propinqua. Ecotoxicol Environ Saf 2008;70:469–74.
Hagger JA, Galloway TS, Langston WJ, Jones MB. Application of biomarkers to assess the
condition of European marine sites. Environ Pollut 2009;157:2003–10.
Hagopian-Schlekat T, Chandler GT, Shaw TJ. Acute toxicity of five sediment-associated
metals, individually and in a mixture, to the estuarine meiobenthic harpacticoid
copepod Amphiascus tenuiremis. Mar Environ Res 2001;51:247–64.
Hammerstrom KK, Ranasinghe JO, Weisberg SB, Oliver JS, Fairey WR, Slattery PN, et al.
Effect of sample area and sieve size on benthic infaunal community condition as-
sessments in California enclosed bays and estuaries. Integr Environ Assess Manage
2012;8:649–58.
Hecht S, Boese BL. Sensitivity of an infaunal amphipod, Eohaustorius estuaries, to acute
waterborne exposures of 4-nonylphenol: evidence of a toxic hangover. Environ
Toxicol Chem 2002;21:816–9.
Hedges LV, Olkin I. Statistical methods for meta-analysis. Orlando, FL, USA: Academic
Press; 1985.
Hinchey EK, Schaffner LC, Hoar CC, Vogt BW, Batte LP. Responses of estuarine benthic
invertebrates to sediment burial: the importance of mobility and adaptation.
Hydrobiologia 2006;556:85–98.
Hinton DE, Baumann PC, Gardner GC, Hawkins WE, Hendricks JD, Murchelano RA, et al.
Histopathologic biomarkers. In: Huggett RJ, Kimerly RA, Mehrle Jr PM, Bergman HL,
editors. Biomarkers: biochemical, physiological and histological markers of anthro-
pogenic stress. Chelsea, MI, USA: Lewis. Publishers; 1992. p. 155–210.
Hong YSH, Kinney KA, Reible DD. Effects of cyclic changes in pH and salinity on metals
release from sediments. Environ Toxicol Chem 2011;30:1775–84.
Hose GC, Murray BR, Park ML, Kehaler BP, Figueira WF. A meta-analysis comparing the
toxicity of sediments in the laboratory and in situ. Environ Toxicol Chem 2006;25:
1148–52.
90 P.M. Chapman et al. / Environment International 55 (2013) 71–91
Huang IB, Keisler J, Linkov I. Multi-criteria decision analysis in environmental sciences:
ten years of applications and trends. Sci Total Environ 2011;409:3578–94.
Hyne RV, Gale SA, King CK. Laboratory culture and life-cycle experiments with the ben-
thic amphipod Melita plumulosa (Zeidler). Environ Toxicol Chem 2005;24:
2065–73.
Hyne RV, Sánchez-Bayo F, Bryan AD, Johnston EL, Mann RM. Fatty acid composition of
the estuarine amphipod, Melita plumulosa (Zeidler): link between diet and fecun-
dity. Environ Toxicol Chem 2009;28:123–32.
Jarvie HP, Jickells TD, Skeffington RA, Withers PJA. Climate change and coupling of mac-
ronutrient cycles along the atmospheric, terrestrial, freshwater and estuarine con-
tinuum. Sci Total Environ 2012;434:252–8.
Kapo KE, Burton Jr GA, De Zwart D, Posthuma L, Dyer SD. Quantitative lines of evidence
for screening-level diagnostic assessment of regional fish community impacts:
a comparison of spatial database evaluation methods. Environ Sci Technol
2008;42:9412–8.
Kemp WM, Boynton WR. Synthesis in estuarine and coastal ecological research: what is
it, why is it important, and how do we teach it? Estuar Coasts 2012;35:1-22.
Khan FR, Misra SK, García-Alonso J, Smith BD, Strekopytov S, Rainbow PS, et al.
Bioaccumulation dynamics and modeling in an estuarine invertebrate following
aqueous exposure to nanosized and dissolved silver. Environ Sci Technol
2012;46:7621–8.
Kirkpatrick AJ, Gerhardt A, Dick JTA, McKenna M, Berges JA. Use of the multispecies
freshwater biomonitor to assess behavioral changes of Corophium volutator (Pallas,
1766) (Crustacea, Amphipoda) in response to toxicant exposure in sediment.
Ecotox Environ Saf 2006;64:298–303.
Krell B, Moreira-Santos M, Ribeiro R. An estuarine mudsnail in situ toxicity assay based
on postexposure feeding. Environ Toxicol Chem 2011;30:1935–42.
Laane RWPM, Slijkerman D, Vethaak AD, Schobben JHM. Assessment of the environ-
mental status of the coastal and marine aquatic environment in Europe: a plea
for adaptive management. Estuar Coast Shelf Sci 2012;96:31–8.
Lemming G, Chambon JC, Binning PJ, Bjerg PL. Is there an environmental benefit from
remediation of a contaminated site? Combined assessments of the risk reduction
and live cycle impact of remediation. J Environ Manage 2012;112:392–403.
Lewis C, Ford AT. Infertility in male aquatic invertebrates: a review. Aquat Toxicol
2012;120–121:79–89.
Linkov I, Loney D, Cormier S, Satterstrom FK, Bridges T. Weight-of-evidence evaluation
in environmental assessment: review of qualitative and quantitative approaches.
Sci Total Environ 2009;407:5199–205.
Linkov I, Welle P, Loney D, Tkachuk A, Canis L, Kim JB, et al. Use of multicriteria deci-
sion analysis to support weight of evidence evaluation. Risk Anal 2011;31:
1211–25.
Liu N, Pan L, Wang J, Yang H, Liu D. Application of the biomarker responses in scallop
(Chlamys farreri) to assess metals and PAHs pollution in Jiaozhou Bay, China. Mar
Environ Res 2012;80:38–45.
Lyons BP, Thain JE, Stentiford GD, Hylland K, Davies IM, Vethaak AD. Using biological
effects tools to define Good Environmental Status under the European Union
Marine Strategy Framework Directive. Mar Pollut Bull 2010;60:1647–51.
Mann RM, Hyne RV, Spadaro DA, Simpson SL. Development and application of a rapid
amphipod reproduction test for sediment-quality assessment. Environ Toxicol
Chem 2009;28:1244–54.
Manyin T, Rowe CL. Chronic exposure of Leptocheirus plumulosus to Baltimore Harbor
sediment: bioenergetic and population-level effects. Mar Environ Res 2006;62:
116–30.
Marsden ID, Wong CHT. Effects of sediment copper on a tube-dwelling estuarine am-
phipod, Paracorophium excavatum. Mar Freshwater Res 2001;52:1007–14.
Martín-Díaz ML, Blasco J, Sales D, DelValls TA. Biomarkers as tools to assess sediment
quality. Laboratory and field surveys. Trends Anal Chem 2004;23:10–1.
Martín-Díaz ML, Blasco J, Sales D, DelValls TA. Biomarkers study for sediment quality
assessment in Spanish ports using the crab Carcinus maenas and the clam Ruditapes
philippinarum. Arch Environ Contam Toxicol 2007;53:66–76.
Martín-Díaz ML, Blasco J, Sales D, DelValls TA. Field validation of a battery of bio-
markers to assess sediment quality in Spanish ports. Environ Pollut 2008a;151:
631–40.
Martín-Díaz ML, Jiménez-Tenorio N, Sales D, DelValls TA. Accumulation and histopath-
ological damage in the clam Ruditapes philippinarum and the crab Carcinus maenas
to assess sediment toxicity in Spanish ports. Chemosphere 2008b;71:1916–27.
Maruya KA, Landrum PF, Burgess RM, Shine JP. Incorporating contaminant bioavailabil-
ity into sediment quality assessment frameworks. Integr Environ Assess Manage
2012;8:659–73.
McClelland JW, Holmes RM, Dunton KH. The Arctic Ocean estuary. Estuar Coasts
2012;35:353–68.
McLeod RJ, Wing SR, Skilton JE. High incidence of invertebrate-chemoautotroph symbi-
oses in benthic communities of the New Zealand fjords. Limnol Oceanogr 2010;55:
2097–106.
McLusky DS, Elliott M. Transitional waters: a new approach, semantics or just muddy-
ing the waters? Estuar Coast Shelf Sci 2007;71:359–63.
McPherson CA, Chapman PM. Copper effects on potential sediment test organisms: the
importance of appropriate sensitivity. Mar Pollut Bull 2000;40:656–65.
MEA (Millenium Ecosystem Assessment). Ecosystems and human well-being: a frame-
work for assessment. Washington, DC, USA: Island Press; 2003.
Melo SLR, Nipper M. Sediment toxicity tests using the burrowing amphipod Tiburonella
viscana (Amphipoda: Platyischnopidae). Ecotox Environ Saf 2007;66:412–20.
Menzie CA, Deardorff T, Booth P, Wickwire T. Refocusing on nature: holistic assessment
of ecosystem services. Integr Environ Assess Manage 2012;8:401–11.
Meysman FJR, Middelburg JJ, Heip CHR. Bioturbation: a fresh look at Darwin's last idea.
Trends Ecol Evol 2006;21:688–95.
Monserrat JM, Martínez PE, Geracitano LA, Amado LL, Martins CMG, Pinho GLL, et al.
Pollution biomarkers in estuarine animals: critical review and new perspectives.
Comp Biochem Physiol C 2007;146:221–34.
Morales-Caselles C, Riba I, Sarasquete C, DelValls TA. Application of a weight of evi-
dence approach to compare the quality of coastal sediments affected by acute
(Prestige 2002) and chronic (Bay of Algeciras) oil spills. Environ Pollut 2008;156:
394–402.
Morales-Caselles C, Riba I, DelValls TA. A weight of evidence approach for quality as-
sessment of sediments impacted by an oil spill: the role of a set of biomarkers as
a line of evidence. Mar Environ Res 2009;67:31–7.
Moreira SM, Moreira-Santos M, Guilhermino L, Ribeiro R. A short-term sublethal in situ
toxicity assay with Hediste diversicolor (Polychaeta) for estuarine sediments based
on postexposure feeding. Environ Toxicol Chem 2005;24:2010–8.
Moreira SM, Moreira-Santos M, Guilhermino L, Ribeiro R. An in situ post exposure feed-
ing assay with Carcinus maenas for estuarine sediment-overlying water toxicity
evaluations. Environ Pollut 2006a;139:318–29.
Moreira SM, Guilhermino L, Ribeiro R. An in situ assay with the microalga
Phaeodactylum tricornutum for sediment-overlying water toxicity evaluations in
estuaries. Environ Toxicol Chem 2006b;25:2272–9.
Moreira SM, Lima I, Ribeiro R, Guilhermino L. Effects of estuarine sediment contamina-
tion on feeding and on key physiological functions of the polychaete Hediste
diversicolor. Laboratory and in situ assays. Aquat Toxicol 2006c;78:186–201.
Moreno-Garrido I, Lubián LM, Jiménez B, Soares AMVM, Blasco J. Estuarine sediment
toxicity tests on diatoms: sensitivity comparison for three species. Estuar Coastal
Shelf Sci 2007;71:278–86.
Neuparth T, Correia AD, Costa FO, Lima G, Costa MH. Multi-level assessment of chronic
toxicity of estuarine sediments with the amphipod Gammarus locusta: I. Biochem-
ical endpoints. Mar Environ Res 2005;60:69–91.
Newman MC, Zhao Y, Carriger JF. Coastal and estuarine ecological risk assessment: the
need for a more formal approach to stressor identification. Hydrobiologia
2007;577:31–40.
NRC. Adaptive management for water resource planning. Committee to assess the U.S.
Army Corps of Engineers methods of analysis and peer review for water resources
project planning. Washington, DC, USA: National Academy Press; 2004.
NRC (National Research Council). Committee on Biological Markers of the National Re-
search Council, biological markers in environmental health research. Environ
Health Perspect 1987;74:3–9.
Nunes-Vaz R. The salinity response of an inverse estuary to climate change and desali-
nation. Estuar Coast Shelf Sci 2012;98:49–59.
O'Brien AL, Keough MJ. Detecting benthic community responses to pollution in estuar-
ies: a field mesocosm approach. Environ Pollut 2013;175:45–55.
O'Higgins TG, Ferraro SP, Dantin DD, Jordan SJ, Chintala MM. Habitat scale mapping of
fisheries ecosystem service values in estuaries. Ecol Soc 2010;15(4):7. [[online]
URL: http://www.ecologyandsociety.org/vol15/iss4/art7/ [accessed September 22,
2012]].
Oliveira M, Maria VL, Ahmad I, Serafim A, Bebianno MJ, Pacheco M, et al. Contamination
assessment of a coastal lagoon (Ria de Aveiro, Portugal) using defence and damage
biochemical indicators in gill of Liza aurata — an integrated biomarker approach.
Environ Pollut 2009;157:959–67.
Pascual M, Borja A, Franco J, Burdon D, Atkins JP, Elliott M. What are the costs and ben-
efits of biodiversity recovery in a highly polluted estuary? Wat. Res. 2012;46:
205–17.
Paul-Pont I, Gonzalez P, Baudrimont M, Jude F, Raymond N, Bourrasseau L, et al. Inter-
active effects of metal contamination and pathogenic organisms on the marine bi-
valve Cerastoderma edule. Mar Pollut Bull 2010;60:515–25.
Perez-Landa V, Simpson SL. A short life-cycle test with the epibenthic copepod Nitocra
spinipes for sediment toxicity assessment. Environ Toxicol Chem 2011;30:1430–9.
Perillo GME. Definitions and geomorphic classifications of estuaries. In: Perillo GME,
editor. Geomorphology and sedimentology of estuaries. Developments in
sedimentologyNew York, NY, USA: Elsevier; 1995. p. 17–47.
Peters C, Ahlf W. Reproduction of the estuarine and marine amphipod Corophium
volutator (Pallas) in the laboratory for toxicity testing. Chemosphere 2005;59:
525–36.
Pfeifer S, Schiedek D, Dippner JW. Effect of temperature and salinity on acetylcholinesterase
activity, a common pollution biomarker, in Mytilus sp. from the south-western Baltic
Sea. J Exp Mar Biol Ecol 2005;320:93-103.
Picado A, Bebianno MJ, Costa MH, Ferreira A, Vale C. Biomarkers: a strategic tool in the as-
sessment of environmental quality of coastal waters. Hydrobiologia 2007;587:79–87.
Piva F, Ciaprini F, Onorati F, Benedetti M, Fattorini D, Ausili A. Assessing sediment hazard
through a weight of evidence approach with bioindicator organisms: a practical
model to elaborate data from sediment chemistry, bioavailability, biomarkers and
ecotoxicological bioassays. Chemosphere 2011;83:475–85.
Polasky S, Carpenter SR, Folke C, Keeler B. Decision-making under great uncertainty:
environmental management in an era of global change. TREE 2011;26:398–404.
Ré A, Rodrigues AM, Quintino V. Acute toxicity testing with the European marine amphi-
pod Corophium multisetosum. Hydrobiologia 2007;587:89–99.
Ré A, Freitas R, Sampaio L, Rodrigues AM, Quintino V. Estuarine sediment acute toxicity
testing with the European amphipod Corophium multisetosum Stock, 1952.
Chemosphere 2009;76:1323–33.
Remane A. Die Brackwasserfauna. Verh Dtsch Zool Ges 1934;36:34–74.
Riba I, Forja J, Gómez-Parra A, DelValls A. Sediment quality in littoral regions of the Gulf
of Cádiz: a triad approach to address the influence of mining activities. Environ
Pollut 2004;132:341–53.
Riba I, Blasco J, Jiménez-Tenorio N, González de Canales ML, DelValls TA. Heavy-metal bio-
availability and effects: II. Histopathology–bioaccumulation relationships caused by
mining activities in the Gulf of Cádiz (SW, Spain). Chemosphere 2005;58:671–82.
 P.M. Chapman et al. / Environment International 55 (2013) 71–91
Rosen G, Chadwick DB, Burton GA, Taulbee WK, Greenberg MS, Lotufo GR, et al. A sedi-
ment ecotoxicity assessment platform for in situ measures of chemistry,
bioaccumulation and toxicity. Part 2: integrated application to a shallow estuary. En-
viron Pollut 2012;162:457–65.
Rubal M, Guilhermino LM, Medina MH. Individual, populations and community level
effects of subtle anthropogenic contamination in estuarine meiobenthos. Environ
Pollut 2009;157:2751–8.
Rubal M, Guilhermino LM, Medina MH. Two strategies to live in low chronic pollution
estuaries: the potential role of lifestyle. Ecotox Environ Saf 2011;74:1226–31.
Santos IR, Eyre BD, Huettel M. The driving forces of porewater and groundwater flow in
permeable coastal sediments: a review. Estuar Coastal Shelf Sci 2012;98:1-15.
Scarlett A, Rowland SJ, Canty M, Smith EL, Galloway TS. Method for assessing the
chronic toxicity of marine and estuarine sediment-associated contaminants using
the amphipod Corophium volutator. Mar Environ Res 2007;63:457–70.
Scharler UM. Ecosystem development during open and closed phases of temporarily
open/closed estuaries on the subtropical east coast of South Africa. Estuar Coast
Shelf Sci 2012;108:119–31.
Schlekat CE, Decho AW, Chandler GT. Bioavailability of particle-associated silver, cad-
mium, and zinc to the estuarine amphipod Leptocheirus plumulosus through die-
tary ingestion. Limnol Oceanogr 2000;45:11–21.
Schlenk D, Lavado R. Impacts of climate change on hypersaline conditions of estuaries
and xenobiotic toxicity. Aquat Toxicol 2011;105S:78–82.
Schubert H, Feuerpfeil P, Marquardt R, Telesh I, Skarlato S. Macroalgal diversity along
the Baltic Sea salinity gradient challenges Remane's species-minimum concept.
Mar Pollut Bull 2011;62:1948–56.
Schwarzenbach RP, Gschwend PM, Imboden DM. Environmental organic chemistry
2nd ed. Hoboken, NJ, USA: Wiley; 2002.
Serafim A, Company R, Lopes B, Fonseca VF, Franc¸ S, Vasconcelos RP, et al. Application
of an integrated biomarker response index (IBR) to assess temporal variation of
environmental quality in two Portuguese aquatic systems. Ecol Indic 2012;19:
215–25.
Shugart LR, Bickham J, Jackim G, McMahon G, Ridley W, Stein J, et al. DNA alterations.
In: Huggett RJ, Kimerly RA, Mehrle Jr PM, Bergman HL, editors. Biomarkers: bio-
chemical, physiological and histological markers of anthropogenic stress. Chelsea,
MI, USA: Lewis Publishers; 1992. p. 155–210.
Simpson SL, Spadaro DA. Performance and sensitivity of rapid sublethal sediment tox-
icity tests with the amphipod Melita plumulosa and copepod Nitocra spinipes. Envi-
ron Toxicol Chem 2011;30:2326–34.
Smith JT, Walker LA, Shore RF, dit Durell SEA le V, Howe PD, Taylor M. Do estuaries pose
a toxic contamination risk to wading birds? Ecotoxicology 2009;18:906–17.
Soares S, Moreira S, Andrade S, Guilhermino L, Ribeiro R. Freshwater–saltwater interface
and estuarine sediment in situ assays based on post-exposure feeding of chironomids
and polychaetes. Estuaries 2005;28:314–9.
Sparrevik M, Barton DN, Bates ME, Linkov I. Use of stochastic multi-criteria decision
analysis to support sustainable management of contaminated sediments. Environ
Sci Technol 2012;46:1326–34.
Stahl RG, Bingman TS, Guiseppi-Elie A, Hoke RA. What biomonitoring can and cannot
tell us about causality in human health and ecological risk assessments. Human
Ecol Risk Assess 2010;16:74–86.
Stumm W, Morgan JJ. Aquatic chemistry. Chemical equilibria and rates in natural
waters 3rd ed. New York, NY, USA: Wiley; 1996.
Sumner SCJ, Fennell TR. Biomarkers, omics, and species comparisons. Human Ecol Risk
Assess 2007;13:111–9.
Sun J, Wang M-H, Ho Y-S. A historical review and bibliometric analysis of research on
estuary pollution. Mar Pollut Bull 2012;64:13–21.
Suter II GW, Cormier SM. Why and how to combine evidence in environmental assessments:
weighing evidence and building cases. Sci Tot Environ 2011;409:1407–17.
Suter II GW, Norton SB, Fairbrother A. Individuals versus organisms versus populations
in the definition of ecological assessment endpoints. Integr Environ Assess Manage
2005;1:397–400.
Syvitski JPM, Morehead MD, Bahr D, Mulder T. Estimating fluvial sediment transport:
the rating parameters. Water Resour Res 2000;36:2747–60.
91
Thain JE, Vethaak D, Hylland K. Contaminants in marine ecosystems: developing an in-
tegrated indicator framework using biological effects techniques. ICES J Mar Sci
2008;65:1508–14.
Thompson B, Weisberg SB, Melwani A, Lowe S, Ranasinghe JA, Cadien DB, et al. Low levels
of agreement among experts using best professional judgment to assess benthic con-
dition in the San Francisco Estuary and Delta. Ecol Indic 2012;12:167–73.
Turner A, Millward GE. Suspended particles: their role in estuarine biogeochemical
cycles. Estuar. Coast. Shelf Sci. 2002;55:857–83.
Turner A, Rawling MC. The influence of salting out on the sorption of neutral organic
compounds in estuaries. Water Res 2001;35:4379–89.
Turner A, Martino M, le Roux SM. Trace metal distribution coefficients in the Mersey
estuary, UK: evidence for salting out of metal complexes. Environ Sci Technol
2002;36:4578–84.
Turner A, Le Roux SM, Millward GE. Speciation and partitioning of cadmium and zinc in
two contrasting estuaries: the role of hydrophobic organic matter. Limnol
Oceanogr 2004a;49:11–9.
Turner A, Millward GE, Le Roux SM. Significance of oxides and particulate organic mat-
ter in controlling trace metal partitioning in a contaminated estuary. Mar Chem
2004b;88:179–92.
USEPA (U.S. Environmental Protection Agency). Causal Analysis/Decision Information
System (CADDIS). Washington, DC, USA: Office of Research and Development;
2010 [www.epa.gov/caddis].
Valavanidis A, Vlahogiannia T, Dassenakis M, Scoullos M. Molecular biomarkers of
oxidative stress in aquatic organisms in relation to toxic environmental pollutants.
Ecotox Environ Saf 2006;64:178–89.
van den Heuvel-Greve M, Postma J, Jol J, Kooman H, Dubbeldam M, Schipper C, et al. A
chronic bioassay with the estuarine amphipod Corophium volutator: test method
description and confounding factors. Chemosphere 2007;66:1301–9.
van der Oost R, Beyer J, Vermeulen NPE. Fish bioaccumulation and biomarkers in envi-
ronmental risk assessment: a review. Environ Toxicol Pharmacol 2003;13:57-149.
Veiga P, Rubal M, Arenas F, Incera M, Olabarria C, Sousa-Pinto I. Does Carcinus maenas
facilitate the invasion of Xenostrobus secures? J Exp Mar Biol Ecol 2011;406:14–20.
Veríssimo H, Lane M, Patrício J, Gambito S, Marques JC. Trends in water quality and
subtidal benthic communities in a temperate estuary: is the response to restora-
tion efforts hidden by climate variability and the Estuarine Quality Paradox?
Ecol. Indic. 2013;24:56–67.
Vinagre C, Salgado JP, Mendonça V, Cabral H, Costa MJ. Isotopes reveal fluctuation in
trophic levels of estuarine organisms, in space and time. J Sea Res 2012;72:49–54.
Wall DH, editor. Sustaining biodiversity and ecosystem services in soils and sediments.
Washington, DC, USA: Island Press1-55963-760-9; 2004.
Weed DL. Weight of evidence: a review of concept and methods. Risk Anal 2005;25:
1545–57.
Wen L, Shiller A, Santschi PH, Gill G. Trace element behavior in Gulf of Mexico estuar-
ies. In: Bianchi TS, Pennock JR, Twilley RR, editors. Biogeochemistry of Gulf of Mexico
estuaries. New York, NY, USA: John Wiley; 1999. p. 303–46.
Werner I, Deanovic LA, Markiewicz D, Khamphanh M, Reece CK, Stillway M, et al. Mon-
itoring acute and chronic water column toxicity in the northern Sacramento–San
Joaquin estuary, California, USA, using the euryhaline amphipod, Hyalella azteca:
2006 to 2007. Environ Toxicol Chem 2010;29:2190–9.
Whitfield AK, Elliott M, Basset A, Blaber SJM, West RJ. Paradigms in estuarine ecology —
a review of the Remane diagram with a suggested revised model for estuaries.
Estuar Coast Shelf Sci 2012;97:78–90.
WHO (World Health Organization). International Programme on Chemical Safety
(IPCS). Biomarkers and risk assessment: concepts and principles, 155. Environ-
mental Health Criteria; 1993[Geneva, Switzerland].
Williams DD, Williams NE. Aquatic insects in an estuarine environment: densities, dis-
tribution and salinity tolerance. Freshw Biol 1998;39:411–21.
Zelikoff JT, Carlson E, Li Y, Raymond A, Duffy J, Beaman JR, et al. Immunotoxicity bio-
markers in fish: development, validation and application for field Studies and
risk assessment. Human Ecol. Risk Assess 2002;8:253–63.
Zielinski S, Pörtner H-O. Oxidative stress and antioxidative defense in cephalopods: a
function of metabolic rate or age? Comp Biochem Physiol B 2000;125:147–60.