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Estuarine, Coastal and Shelf Science 94 (2011) 306e314

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Estuarine, Coastal and Shelf Science

journal homepage: www.elsevier .com/locate/ecss

Challenging paradigms in estuarine ecology and management

M. Elliott a,*, A.K. Whitfield b

a Institute of Estuarine & Coastal Studies, University of Hull, Hull HU6 7RX, UKb South African Institute for Aquatic Biodiversity, Grahamstown 6140, South Africa

a r t i c l e i n f o

Article history:Received 2 May 2011Accepted 21 June 2011Available online 3 July 2011

Keywords:estuariesparadigmsecologymanagement

* Corresponding author.E-mail addresses: Mike.Elliott@hull.ac.uk (M. El

(A.K. Whitfield).

0272-7714/$ e see front matter � 2011 Elsevier Ltd.doi:10.1016/j.ecss.2011.06.016

a b s t r a c t

For many years, estuarine science has been the ‘poor relation’ in aquatic research e freshwater scientistsignored estuaries as they tended to get confused by salt and tides, and marine scientists were morepreoccupied by large open systems. Estuaries were merely regarded by each group as either river mouthsor sea inlets respectively. For the past four decades, however, estuaries (and other transitional waters)have been regarded as being ecosystems in their own right. Although often not termed as such, this hasled to paradigms being generated to summarise estuarine structure and functioning and which relate toboth the natural science and management of these systems. This paper defines, details and affirms theseparadigms that can be grouped into those covering firstly the science (definitions, scales, linkages,productivity, tolerances and variability) and secondly the management (pressures, valuation, health andservices) of estuaries. The more ‘science’ orientated paradigms incorporate the development and types ofecotones, the nature of stressed and variable systems (with specific reference to resilience and redun-dancy), the relationship between generalists and specialists produced by environmental tolerance, therelevance of scale in relation to functioning and connectivity, the sources of production and degree ofproductivity, the biodiversity-ecosystem functioning and the stress-subsidy debates. The more‘management’ targeted paradigms include the development and effects of exogenic unmanaged pres-sures and endogenic managed pressures, the perception of health and the ability to manage estuaries(related to internal and external influences), and the influence of all of these on the production ofecosystem services and societal benefits.

� 2011 Elsevier Ltd. All rights reserved.

1. Introduction

Following the recent review by Whitfield and Elliott (in press),an estuary can be defined as ‘a semi-enclosed coastal body of waterwhich is connected to the sea either permanently or periodically, hasa salinity that is different from that of the adjacent open ocean due tofreshwater inputs, and includes a characteristic biota’. In addition,estuaries are now regarded as being an example of ‘transitionalwaters’, a term which includes lagoons, rias, etc. (Elliott andMcLusky, 2002; McLusky and Elliott, 2007). While there has beenan increasing number of papers devoted to estuarine science andmanagement, as shown in this journal (e.g. Neto et al., 2008), therehas long been a debate about the characteristics of estuaries andtheir functioning (Hume et al., 2007; Dürr et al., 2011). This reviewfocuses primarily on northern and southern temperate systems,although it is envisaged that much of the discussion which followswill apply to estuaries in other parts of the world.

liott), a.whitfield@saiab.ac.za

All rights reserved.

This paper aims to present a set of paradigms relating to bothnorthern and southern hemisphere estuaries. Here the term para-digm is used to mean a set of concepts or accepted philosophiesthat define a field of science which has been developed over thehistory of a field, but which are amenable to testing via the scien-tific method using hypothesis generation. Kuhn (1970) considersthat a scientific paradigm can cover concepts and observations,questions and hypotheses and the interpretation of field, laboratoryand modelling observations, measurements and outcomes. Hencethere must be the ability to prove or disprove the paradigms or totest for deviations from what is accepted. Here we take the viewthat paradigms do not have to be mutually exclusive and theyshould comprise a set of unifying concepts central to the scienceand management.

It is widely acknowledged that paradigms can develop fromacomment inapublishedpaper (withall its caveats) tobecomeahardfact (without caveats) by the time the ‘fact’ has been put into a book.The ‘fact’ then keeps being repeated, without it being tested rigor-ously, and is thus reinforced as a ‘fact’ within the scientific commu-nity.Hence there is aneed to reject, reaffirmor test currentparadigmsinestuarine ecologyandmanagement. Furthermore, there is theneed

M. Elliott, A.K. Whitfield / Estuarine, Coastal and Shelf Science 94 (2011) 306e314 307

to determine paradoxes within or between paradigms and also todeterminewhetheraparadigmholds foragivengeographical area, anestuary type or is more widely applicable. By definition, a paradigmshould hold across the discipline, and hence paradigms need to betested and rejected when found not to hold true.

There is the constant need to review paradigms in the light ofnew information and understanding, and there is also a need toacknowledge that they sometimes challenge our view of the topicand may even give new directions for future research. We take theview that a paradigm should stand up to scrutiny and if it fails thattest then it should be discarded. We also contend that paradigmsare challenging because they are generally structured around somefundamental aspect of science (often ecological functioning in thecase of estuaries).

The paradigms outlined below have been gathered by ourreading, refereeing, editing and writing of estuarine papers, chap-ters and books over many decades. While writing this review, westarted with 35 statements and refined that to 20 after decidingthat some applied to estuaries in one part of the world but notanother. From that second iteration it was decided to merge andrefine these 20 to the final set of eight given here. Those finalparadigms were then presented at the April 2011 internationalsymposium of ECSA/SAMSS held in Grahamstown, South Africa,and then refined further using discussions and feedback.

The proposed paradigms of course need supporting and, whilereferences are given here where possible, this is occasionallydifficult for those paradigms which by their very nature tend to beobscure in terms of actual origin. This contrasts to formulae, indicesand laws which are usually linked to a particular published paper.Accordingly, here we detail, expand, propose, define, comment andchallenge and/or affirm the selected paradigms. Other estuarinescientists may disagree or have additional paradigms but thispreliminary list is presented to stimulate debate and discussion.

2. Natural science-based paradigms

2.1. Definitions, scales, ecotones and linkages2.1.1. Paradigm 1

An estuary is an ecosystem in its own right but cannot functionindefinitely on its own in isolation and that it depends largely on otherecosystems, possibly more so than do other ecosystems.

(a) Interpretation/meaningAn ecosystem can be defined as: ‘a dynamic complex of plant,animal and micro-organism communities and their non-livingenvironment interacting as a functional unit’ (CBD, 2000). Mostestuarine characteristics relate to connections and connectivitywith freshwater andmarine areas; therefore for a system to be anestuary it has, by definition, to depend on other systems (Dürret al., 2011). Of course, very few large ecosystems are self-contained and they all have some degree of interlinking. Nonatural ecosystem is completely closed (e.g. the rainfall cycleaffects just about every ecosystem, it is global and not closed) buton an open/closed scale, estuaries are mostly very ‘open’ systemsgiven their strong connectivity with both the riverine andmarineenvironments (Gómez-Gesteira et al., 2003; Kremer et al., 2010).While all ecosystems are linked to the atmosphere, no othershave simultaneous connectivity to freshwater catchment andterrestrial influences, the atmosphere andmarine systemse thusin many respects estuaries could be regarded as multi-interfacesystems, i.e. ecosystems with multiple major influences andboundaries. Whilst they are open, however, they are ecosystemswith their own specific characteristics and exist because of theiralmost continuous links with rivers or the sea or both. However,for those estuaries that are occasionally closed by sand bars

because of low river flows, the available evidence suggests thatan intermittent systemwill continue to function as an estuary aslong as it opens on occasions (Whitfield et al., 2008).

(b) Comments/relevance/supportWe contend that an ecosystem can be defined by its paradigms.There has long been a debate on what is an estuary, partlybecause there is greater variability in the structure and nature ofestuaries around the world than there is for example betweentropical forests around the world e hence the ongoing debatearoundwhat is an estuary (Elliott andMcLusky, 2002;Whitfield,2005).Northern hemisphere scientists approached the definition of anestuary based on high freshwater input systems (see Elliott andMcLusky, 2002, and references therein for a discussion of defi-nitions of estuaries), whereas southern hemisphere scientistshave to deal with a variety of systems, many of which have verylimited riverine inputs associated with arid climates (Potteret al., 2010). Arguably the largest problem confronting thosesystems is the lack of freshwater inputs which may covermedium or long periods, hence giving rise to closed systemsand/or hypersaline areas. It is emphasised that while arid areasoccur in the northern regions, and thus create particular types ofestuaries which behave similarly to arid zone estuaries world-wide, these are more common in the south. In addition, theproportionally larger number of intermittently open estuaries inthe southern hemisphere also tends to lead to a divergencebetween the north and south on what constitutes a typicalestuary. The microtidal nature of many southern hemispherecoasts is also very different to the macrotidal characteristics ofmany northern hemisphere coasts (where most estuarineresearch has been conducted). Thus the significant marineinfluence on large North American and European estuariesovershadows the more limited marine influence on southernhemisphere estuaries.In contrast to many southern systems, many northern ones areusually open or atmost only partly closed by ebb-tide deltas and/orbarrier islands; hence they tend tohave constant linksbetweensea and freshwaters, whereas many southern systems do not,especially in southern Africa and Australia. Evidence fromtemporarilyclosedestuaries in thesouthernhemisphere suggeststhat estuaries can function in isolation for many years (duringprolonged droughts) and that they can ‘bounce back’ very quicklyonce the connectivity with marine and freshwater systems isrestored. For example, the East Kleinemonde Estuary, continu-ously monitored since the early 1990s (Whitfield et al., 2008), iscurrently experiencing amore than 3-year effective closed phase,yet both marine and estuarine fish species appear to bemaintaining their populations and ecological balance very well.

2.1.2. Paradigm 2As ecosystems, estuaries are more influenced by scale than any

other aquatic system; their essence is in the connectivity across thevarious scales and within the water body they are characterised by oneor more ecotones.

(a) Interpretation/meaningEstuaries, as with all ecosystems, respond to processes oper-ating at different scales but this paradigm suggests that forestuaries the scales range from internal (within estuary), to local(between estuaries, between estuary-river, between estuary-sea), to larger biogeographical scales. For example, the latterincludes the links between polar breeding grounds fortemperate estuarine wading birds and the migrations from theopen ocean to coastal regions for eels.

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If an ecotone is defined (Attrill and Rundle, 2002) as beinga transition/gradient between two systems, then estuaries canbe regarded as having several ecotones e into the estuary fromadjacent freshwater catchments, out of the estuary to themarine/coastal area, laterally from the supratidal region into thelittoral margins, vertically from the air interface into the surfacewaters, from the water column into the estuary bed, and withdepth/stratification throughout the water column. The relativesize (spatial dimension), influence and temporal presence ofeach of these ecotones varies with locality and type of estuary.While classically an ecotone would be expected to have anincreased biodiversity due to the mixing of two adjacentsystems, either this does not appear to occur in estuarineecotones or it has not been documented (Attrill, 2002).

(b) Comments/relevance/supportThe scales of both the estuary size and the catchment area ofmany northern hemisphere estuarine systems appear to bemuch larger and cover a wider area than those in most southernhemisphere situations. This may be related to the larger riverinedischarges (on average) into the northern hemisphere estuarieswhich accentuate the size of the transitional waters at both thehead and mouth regions of these systems (Milliman, 2001).The scales of temperature variation in estuaries are also muchlarger in the northern hemisphere because the continentswhere most studies have been conducted are at higher lati-tudes than equivalent systems in the southern hemisphere.For example, the Rhine is a large estuary with an internationalcatchment whose organisms are dependent on an area fromthe poles (for the overwintering wading birds) to the westernAtlantic/Sargasso Sea (for eels). Although some of the largerAfrican temperate estuaries in the southern hemisphere hostpalaeoarctic migrant bird species from Europe and Asia, andanguillid eels from as far a field as Madagascar, none of thesesystems freeze over in winter as occurs in some northerntemperate estuaries (Kuzyk et al., 2008).The importance andpresence of ecotonesmay relate to the size ofthe estuaries and their catchment inputs. Thus many smallersouthern estuaries (and the smaller estuaries in northern areas,for example some of those along the coast of northern Spain)behave as having one main ecotone (estuarine-marine) whereasthe larger and deeper northern estuaries with large perennialriverine inflows show all the characteristics and ecotonesmentioned above. Hence, for estuaries stretching >100 km,several kilometres in width and up to tens of metres deep,ecotones can develop at the head, mouth, edges and with depth.Even though these ecotones will migrate (i.e. the one at the headmay migrate further down into the estuary under high flowconditions) they still are preserved spatially. Closed-mouthestuaries lose their longitudinal ecotones (estuarine-marineand estuarine-freshwater) for the period that they are closed,which may be seasonally or for up to several years duringextended droughts. Well-mixed estuaries conceivably will havelost their lateral and vertical ecotones and these aremore likely tooccur in small shallow temporarily open/closed southern hemi-sphere systems (Whitfield et al., 2008). In addition, for somesmall temporarily closed estuaries there is sometimes no ecotonebetween the freshwater environment and marine environmentand estuary due to a temporary cessation of river flow during thedry season (Taljaard et al., 2009; Potter et al., 2010). For openestuaries, the presence and influence of ecotones may vary dailywith diurnal tides, on a spring-neap cycle, seasonally or inter-annually. Hence the paradigm suggests that while ecotones donot have to be present continually, they are central to overallestuarine functioning.

2.2. Hydromorphological and organic functioning2.2.1. Paradigm 3

Hydromorphology is the key to understanding estuarine func-tioning but these systems are always influenced by salinity (and theresulting density/buoyancy currents) as a primary environmentaldriver.

(a) Interpretation/meaningHydromorphology is regarded and can be interpreted as rep-resenting the links between the sediments and suspendedsediment, water movements and tidal balance, all of whichinfluence the estuarine biota and are superimposed on theunderlying geology/geomorphology of the system (Gray andElliott, 2009; Nicolas et al., 2010). Hydromorphology will bethe primary determinant for the residence time of water withinan estuary and this will have a major impact on the ecologicalfunctioning of both northern and southern hemisphere systems(Chicharo and Chicharo, 2006; Haines et al., 2006; Wolanski,2007).Salinity is a primary factor (and its dominant influence suggestseverything else is secondary) but most estuary-associatedspecies are highly euryhaline (see also Bulger et al., 1993). Riverflow, especially in the context of estuarine morphology, is also ofhigh importance and a key component in the understanding ofhydromorphology (Gómez-Gesteira et al., 2003). Based on thehydromorphology, the estuarine characteristics and thus pres-sures on the biota are therefore shaped by the relative influenceof the tides and river inputs, the creation of a TurbidityMaximumZone (especially in northern hemisphere systems), and in turnpoor water column light conditions preventing/limiting primaryproduction (Burford et al., 2011). The density/buoyancy drivencurrents produced by water bodies of different salinity (andtemperature) interacting appear to be central to the hydrody-namic functioningof all estuaries although theydohavedifferingstrengths of influence (Wolanski et al., 2004; Uncles, 2010).Furthermore, the net result of the tidal and freshwater influencescreates the flushing rate and its corollary the residencetime (Monsen et al., 2002), both of which influence in turn thesalinity, the ability to retain nutrients, the dispersal of certainstages of benthic organisms and plankton and the widerconnectivity between systems (de Brauwere et al., 2011).

(b) Comments/relevance/supportHydromorphology is a major driver of estuarine ecosystemfunctioning in that it can lead to both changed salinity condi-tions and/or the physical removal of organisms. There are manyexamples of strong river flow driving euryhaline marine fishesout of more linear estuaries (Whitfield and Harrison, 2003),even though they can survive in freshwater or oligohalinewaters for prolonged periods (Ter Morshuizen et al., 1996). Thismay suggest a hierarchy of the influence of physical factors andthat the hydromorphology influence may be more of a globalparadigm than that of salinity for certain systems (Marais, 1982).The hydromorphology will influence sediment inputs fromriverine systems, as well as tidal pulsing and the creation of highturbidity areas in many estuaries. This in turn will affect thewater column primary productivity and perhaps the key ques-tion here is whether turbidity is more important in structuringestuarine assemblages than light, or whether the two must bedealt with together. The level of turbidity has the potential todetermine whether a system becomes eutrophic by retainingnutrients or whether it merely exports nutrients to the receivingcoastal waters (de Jonge and Elliott, 2002). Even highly turbidestuaries such as St Lucia (South Africa), that are severely lightlimited for much of the time (Cyrus, 1988), are biologically

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diverse and productive ecosystems. Some northern hemisphereestuaries also have high levels of suspended solids and/orphytoplankton, with tidal resuspension of microphytobenthosand benthic organic material also contributing to elevatedturbidity levels (Bodineau et al., 1998; Fries et al., 2007). Forexample, the Humber Estuary, eastern England, consistently hasturbidity levels exceeding 5 g l�1 thus influencing its watercolumn productivity (Boyes and Elliott, 2006).In shallow estuarine systems (e.g. <5 m depth), water columnmixing is often wind-driven and therefore phytoplankton andmicrophytobenthos are brought to the water surface regularlydue to vertical circulation (Grange and Allanson, 1995; de Jongeand Van Beusekom, 1995). In general, estuaries in both thenorthern and southern hemispheres are more turbid than clear,hence the lack of colour in invertebrates, fishes, etc. in bothhemispheres. From a light perspective, the functioning of mosttemperate estuaries during the winter is not affected as thereare sufficiently high light intensities for photosynthesis in thewater column and by epiphytes to occur. In addition, as dis-cussed below, the detrital inputs associated with estuaries meanthat the annual production cycle is more dampened and lesspronounced than in open sea systems (i.e. spring and autumnphytoplankton blooms are not as pronounced in estuaries butdetritus is present in large quantities throughout the year forconsumers).

2.2.2. Paradigm 4Although estuaries behave as sources and sinks for nutrients and

organic matter, in most systems allochthonous organic inputs domi-nate over autochthonous organic production.

(a) Interpretation/meaningWhile estuaries have an abundance of autochthonous producingfringing areas (e.g. reedbeds, seagrass meadows, mangroves andsaltmarshes), they also receive large amounts of organic mate-rial from riverine primary producers, the sea and even fromanthropogenic waste (Abrantes and Sheaves, 2010; Howe andSimenstad, 2011). Allochthonous organic matter and nutrientsflow into an estuary mainly from the catchment and adjacentwetlands and may be retained there, thus fuelling a detritus-based system. Once in the system, depending on its flushingcharacteristics, some of the materials may also flow to theadjacentmarine area via the estuarine plume or be redistributedwithin the estuary by tidal action (Baird et al., 1987; Whitfield,1988).The ecomorphometry of an estuary (regardedhere as the physicalshape of the estuary but influenced and modified by organismsand their influence on their habitats) is likely to be the maindeterminant of the amount of authochthonous and allochtho-nous inputs retained within a system (Lin et al., 2006). Channel-like estuaries are likely to be poor sinks for nutrients and organicmatter whereas lacustrine, segmented or compartmentalisedestuaries are more likely to retain much of these products, evenunder high river flow conditions. It is important to note that thedelivery of nutrients and organics to any estuary from a river, aswell as exchanges between the estuary andmarine environment,does not usually occur at a constant rate but are pulsed (Odumet al., 1995) such that most may be delivered in a small numberof high flow events; this has been termed the pulsing paradigmby Odum (2002).

(b) Comments/relevance/supportSystems in both the northern and southern hemispheres act as‘detritus traps’ of both allochthonous and autochthonousproduction. Although the proportion/balance between the two

sources will vary on both a temporal and spatial scale, thisphenomenon occurs in estuarine systems in both hemispheres(Baird and Ulanowicz, 1993).Southern hemisphere estuaries that have a closed-mouth phaseare the ultimate sink and, when they burst open, usuallyfollowing river flooding, they are then a primary source of largequantities of nutrients and organic matter to the adjacent seaarea. This process is particularly important in seas with lownutrient levels (e.g. the east coast of southern Africa), but notwhere seas have high nutrient levels (e.g. the west coast ofsouthern Africa). Many northern hemisphere estuaries are largesources and sinks for nutrients and organic matter by virtue oftheir size, high riverine inputs and broad/deep mouth regions(Boyes and Elliott, 2006). Estuaries entering the Mediterraneanare important sources of nutrients for those often oligotrophicareas, whereas estuaries entering the north-west Atlantic maynot necessarily have the same impact.Whilst all estuaries are sources of organic matter to adjacentcoastal zones, there are differences between a constant input tothe sea with uniform flows, and those systems where pulsedinputs can transfer a major nutrient and organic input in a singlespate. Therefore the source-sink magnitudes are linked tohydromorphology constraints and forcing factors, e.g. wetclimatic periods due to the North Atlantic Oscillation or El Niño/La Niña can both deliver large amounts of catchment nutrientsinto estuaries and the adjacent ocean, as well as flush accu-mulated nutrients and organic matter from these systems.The ability of an estuary to convert nutrients to organic matterdepends primarily on the residence time and light regime, e.g.a short residence time (caused by a high tidal range and/orfreshwater flushing) and high turbidity will result in nutrientsentering the system being exported to the adjacent coast beforehaving the opportunity to be used by plants within the estuary.Conversely, an increased residence time favours autochthonousproduction and can even result in phytoplankton or flagellateblooms developing within an estuary (Hilmer and Bate, 1990).

2.3. Variability, resilience and redundancy2.3.1. Paradigm 5

Estuaries are physico-chemically more variable than other aquaticsystems but estuarine communities are less diverse taxonomically andthe individuals are more physiologically adapted to environmentalvariability than equivalent organisms in other aquatic systems.

(a) Interpretation/meaningSalinity and temperature can change greatly over tidal cycles;this is especially the case in temperate northern estuaries butalso for southern ones over very long cycles of opening andclosing. This high variability results in estuaries being biolog-ically much less diverse than equivalent aquatic ecosystemselsewhere (e.g. coral reefs). However, those organisms living inestuaries have an inherent ecological tolerance of environ-mental variability, such that these systems can absorb naturaland anthropogenic stress more effectively than other aquaticecosystems. Consequently estuaries and estuarine organismshave a high resilience to change when compared to the situ-ation in more stable aquatic environments.The strong concurrent spatial and temporal gradients andvariability in salinity (and therefore osmotic pressure on theorganisms) and temperature, and in some systems pH and Eh(redox potential changes), thus produce a challenging set ofphysico-chemical variables which leads to a unique aquaticchemistry. Furthermore, this then results in their uniqueecology. The high degree of variability in estuarine systems hasdictated that organisms living in these areas have a greater

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ability to tolerate and recover from stress (as adverse environ-mental conditions) at the individual, population and communitylevels.Redundancy refers to an ability to remove elements and stillfunction, or to have spare capacity, whereas resilience signifiesthe ability to recover from stress-induced change (Elliott et al.,2007; see also Folke et al., 2004, for a discussion of theconcepts). Although estuarine biota are highly resilient tophysico-chemical changes to their environment, there isa limited pool of species from which to draw should extremeconditions result in the loss of only a few species from thesystem, i.e. the degree of inter-specific redundancy in estuariesis relatively low when compared to that found in many marinesystems (Hughes et al., 2005). However, the large populations ofthe relatively few species present may mean that intra-specificredundancy is high.Ecological redundancy in estuaries has yet to be tested in rela-tion to the removal of organisms within a population, of specieswithin a community, or of communities within habitats. Studiesof these aspects are rare (Duffy et al., 2001) but indications arethat redundancy may differ between biotic groups, especiallythe presence or absence of possible replacement species whenkey taxa are eliminated. For example, in South African estuariesthere are usually only one or two submerged macrophytespecies that can survive particular estuarine conditions. The lossof just one of these species from an estuary often results in thedisappearance of this type of habitat from the system altogether(Whitfield, 1984) (i.e. there is no redundancy). As estuaries ingeneral may be species-poor, caused primarily by the highphysico-chemical variability, the risk of a lack of redundancyneeds to be carefully assessed when placing additional anthro-pogenic pressures on these systems.

(b) Comments/relevance/supportEstuaries in both hemispheres have spatial and temporal vari-ability, related to river flows, tidal inputs, sediment balance anderosion-deposition cycles. Organisms in the intertidal andsupratidal zone of coastal waters also have to withstand vari-ability (of wave action, sediment instability, temporary desic-cation, high and low salinity due to evaporation and rainfall, etc)but this variability is more ‘predictable’ than that occurring inestuaries. Hence estuaries may be regarded paradoxically asbeing ‘constantly variable’ rather than having a consistentvariability! In order to withstand that variability, euryoeciousestuarine organisms should be considered as being morediverse physiologically than stenoecious organisms in theadjacent marine areas.Given the fact that there is already a relatively low speciesdiversity when compared to all the freshwater and marinespecies adjacent to the estuary, the loss of only a few species canhave a major impact on entire food chains, e.g. the collapse ofZostera or Ruppia beds in an estuary usually results in baresediments because there are no other estuarine aquaticmacrophyte species to replace them. Conversely the loss ofseagrasses under eutrophic conditions often leads to replace-ment by opportunistic green algae (Vaudrey et al., 2010). Thistype of succession breakdownwould not happen in a terrestrialenvironment because other species would immediately replacethose lost.The superabundance (hence conferring a large amount oftrophic redundancy) of detritus in estuaries in both hemi-spheres is emphasised by Blaber (1976) who showed that themugilid fishes (detritivores) are all targeting detritus (particu-late organic matter) as a primary food source, with little dietaryseparation between the species. One of the hypotheses arising

from that work was that there is a possible excess supply ofdetritus to estuarine systems, thus minimising competitiveinteractions between detritivores. The superabundance ofdetritus leads to a general acceptance that estuaries are ‘rich’ indetritus (Flindt et al., 2007) and that many animals in estuariesare detritivores. Hence the dominance by detritivores,comprising both invertebrates and fishes, is an underlyingfeature of most estuaries and invertebrate detritivores coversbivalve suspension feeders and epibenthic, benthic and infaunaldetrital consumers (McLusky and Elliott, 2004). In turbidnorthern estuaries, suspension feeders are limited by botha poor phytoplankton food resource and the energetic deficitcaused by excessive gill cleaning. Accordingly, in many of theseestuaries the foodwebs have a central dominant detritivore,either epibenthic crustaceans or infaunal sediment feeders, andhigher predators (fishes and birds) which are generalists in thatthey take any prey they encounter (Elliott et al., 2002).

2.4. Diversity, tolerances, stress, productivity2.4.1. Paradigm 6

Estuaries are systems with low diversity/high biomass/high abun-dance and their ecological components show a diversity minimum inthe oligohaline region which can be explained by the stress-subsidyconcept where tolerant organisms thrive but non-tolerant organismsare absent.

(a) Interpretation/meaningThe diversity of many components is at a minimum in the oli-gohaline area of estuaries (Remane and Schlieper, 1971) wherethere are few species because of the stressful conditions butthose that can survive have a subsidy and create large pop-ulations. The resulting high biomass in this region is related toa large production and inputs of organic matter and nutrients,with the large populations possibly also resulting from a lack ofinter-specific competition.The tolerance range of organisms limit which species can occurin awater body, hence there is a lower diversity in estuaries thanin rivers or at sea. Although diversity is related to the size of anarea and the number of niches, the paradox here is that estua-rine areas are physico-chemically variable, hence there aredifferent water-column niches but only tolerant species cancope with the variability. This results in low diversity (taxo-nomically) but considerable production, rapid growth rates, etc.,by species tolerant of these conditions. Although as yet it needsto be tested, estuaries may show the converse of theBiodiversity-Ecosystem Functioning (BEF) debate (Loreau et al.,2002) in which these systems, despite their lower biodiversity,also produce a high functioning.Because of their physico-chemical variability, many textsemphasise that estuaries are stressful systems for aquaticorganisms (e.g. Saiz-Salinas and González-Oreja, 2000; McLuskyand Elliott, 2004). However, there is a paradox here in that theyare only stressed systems for organisms which cannot toleratethe conditions and thus usually may not survive and thatorganisms adapted to estuarine conditions therefore have idealconditions for survival and growth. Perhaps the central featureof estuarine ecology is that these ecosystems are only stressfulfor those organisms which are not well-adapted for theseconditions; hence for a stenohaline species a euryhaline area islikely to create physiological stress and thus they are likely to beabsent. Furthermore, because of reduced inter-specific compe-tition, any organisms tolerant of estuarine conditions havea subsidy and will thrive in these systems (although intra-specific competition may become more important than inter-specific competition).

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The estuarine biota comprises more generalists than specialists,in terms of physiological tolerances and feeding strategies, andthey tend to be dominated by r-strategists and T-strategistsrather than k-strategists (Gray and Elliott, 2009). It wouldappear that particularly for the zooplankton, zoobenthos andalgae, and especially in the upper reaches (the main salinitytransition areas) most species are r-strategists, i.e. short lived,high turnover, small bodied, fast colonisers; characteristicsrelated not only to the physico-chemical stresses but also thehydrodynamic conditions pertaining to estuaries. For example,even though the lower estuarine areas have k-strategists such asthe tellinid bivalves, the highly variable areas are often domi-nated by oligochaetes (McLusky et al., 1993) and somezooplankton (e.g. Pseudodiaptomus, Eurytemora and Acartia)have rapid reproduction and development to capitalise onchanging estuarine conditions (Jerling and Wooldridge, 1991).There is also a paradox here in that the dominant estuarineorganisms are generalists (euryoecious) in terms of broadtolerances but they are also specialists at surviving highlyvariable conditions. In addition to being generalists in theirphysiology for salinity tolerance, they also very flexible in termsof dietary adaptations to changing food availability and foragingconditions (Whitfield, 1984).

(b) Comments/relevance/supportThe headwaters and oligohaline regions of many northernhemisphere estuaries are dominated by freshwater species butthere is a very poor penetration of freshwater species into theheadwaters of most southern hemisphere estuaries, eventhough this is where the highly productive river-estuaryinterface region is located (Bate et al., 2002). While the Remanepattern (Remane, 1934) is widely quoted as accounting for thisspecies minimum, there is still a need for evidence that can beapplied to all groups of organisms in estuaries, not just thesedentary invertebrate taxa used by Remane (Telesh et al., 2011).Once again, the disjunct at the head (in which river flow ceasesfor long periods) and mouth (closure occurs for long periods) ofmany southern hemisphere estuaries disturbs the continuitydepicted in the Remane diagram (Remane and Schlieper, 1971).The species richness/abundance/biomass model outlined aboveapplies to estuaries in both hemispheres and is related toecological tolerances, the presence of opportunists, the abun-dance of organic material, etc. There is a further paradox that ifbiodiversity is regarded as relating to a taxonomic basis, then forestuaries this needs to be compared to diversity in physiologicalresponse terms. As physiology is a primary driver of the biodi-versity that occurs within estuaries, this, in turn, will affectecosystem functioning in estuaries in both hemispheres. Hence,the Remane diagram is based on the taxonomic diversity ofspecies rather than the diversity of forms using salinity toler-ances or physiology as the criteria.As indicated above, those species that can survive estuarinefluctuations qualify for the ‘subsidy’ that these systems provide.However, within any estuarine community (in both hemi-spheres) there will be those species that qualify for a largesubsidy (e.g. estuarine dependent taxa) and those less adaptedspecies that will receive less of a benefit. If one sets aside thephysiological specialisations required for a life in estuaries, thengeneralists (particularly in terms of dietary flexibility, etc) tendto dominate estuaries in both hemispheres, e.g. there arenumerous examples of fish species in estuaries switching theirdiet in major ways according to food availability (Whitfield,1984). Fish and bird predators especially seem to be generalistand opportunist feeders, hence producing the observedcomplexity of estuarine foodwebs (e.g. Elliott et al., 2002).

Whilst small bodied r-strategists are probably the numericallydominant group in estuaries in both hemispheres, it is possiblethat larger marine migrant k-strategists may predominate ifbiomass is used as the measure (Whitfield, 1990). However, thishas not been properly tested and so warrants further study.Many texts have emphasised that estuaries are naturally‘stressed’ systems (e.g. Dauvin and Ruellet, 2009) but theopposite view could also be argued. The Estuarine FishCommunity Index can sometimes indicate that an estuary is ingood condition (i.e. not artificially stressed) although the use ofselected biomarkers on individual fish can show that the systemis under additional stress (Richardson et al., 2011). Similarly,while stress is often shown at the individual level, it is oftenmore difficult to show this translated to the population orcommunity level (e.g. Borja et al., 2009; García-Alonso et al.,2011). The problem in both hemispheres is that estuarinebiotic communities are adapted to high levels of ‘natural’ stresswhichmakes the assessment of ‘artificial’ (anthropogenic) stressdifficult (Elliott and Quintino, 2007; Dauvin and Ruellet, 2009).Similarly, it is considered that the natural characteristics of anestuary usually mimic those due to anthropogenic stress, the so-called ‘estuarine quality paradox’ (Elliott and Quintino, 2007).

3. Management-based paradigms

3.1. Pressures, valuing, valuation and management3.1.1. Paradigm 7

Estuaries have more human-induced pressures than other systemsand these include both exogenic unmanaged pressures and endogenicmanaged pressures. Consequently their management has to not onlyaccommodate the causes and consequences of pressures within thesystem but, more than other ecosystems, they need to respond to theconsequences of external natural and anthropogenic influences.

(a) Interpretation/meaningJust as estuaries are dependent on ecological scales andprocesses from inside and outside the system, so the manage-ment of estuaries has to accommodate the consequences ofpressures emanating from outside the system (exogenicunmanaged pressures) and the causes and consequences ofpressures from within the system (endogenic managed pres-sures) (Borja et al., 2010; Elliott, 2011). For example, alleviatingeutrophication in an estuary requires managing the conse-quences of nutrients from upstream but within a light regime/mixing environment created by waves and tides, over whichmanagement has no control.Given the pre-eminence of estuaries as favoured sites for urban,port and industrial activities, as well as the anthropogenicpressures emanating from the catchment and marine environ-ment which affect estuarine structure or functioning, then it islikely that estuaries have more pressures than other systems(McLusky and Elliott, 2004). In addition, there are consequencesfor estuaries of global change such as altered rainfall patterns,temperature regime shifts and sea-level rise (Milliman et al.,2008). This again emphasises the importance of scale in estua-rine management, including external influences in catchments(e.g. inflow of nutrients, organisms, water balance) and at sea(e.g. climatic conditions, storm surges, sea-level rise). Again weemphasise that anthropogenic influences are superimposed onto natural influences that already place these ecosystems undera large amount of stress.The nested DPSIR approach is perhaps even more relevant toestuaries than for other systems, and in managing estuaries theEcosystem Approach, which links the natural and socio-economic aspects (e.g. Elliott, 2011), has to be broader than in

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other ecosystems. The DPSIR framework relates to Drivers,Pressures, State Changes, Impacts and Responses (developedfrom OECD, 1993 and expanded in Atkins et al., 2011); eachdriver has a DPSIR cycle and there are many such cycles withinan estuary (navigation/transport, food provision, infrastructurearea, recreation/tourism, etc.), but also there are DPSIR cyclesupstream and at sea which affect those in the estuary. Forexample, demands for food produced by marine fisheries placeadditional pressures on the estuarine community (which is thenursery area for some of these targeted species) and, unlesscontrolled, will have an impact on catches by depleting estua-rine fish stocks. There is also the possibility that reduced marinefish stocks will increase the demand for estuarine sites foraquaculture which will then place increasing pressure on theecological functioning of the estuary.The EcosystemApproach sensu stricto relates tomanagement forboth ecological and socio-economic benefits (Elliott, 2011).Hence, in the case of applying this to an estuary then the naturaland social aspects in the catchment (freshwater and terrestrialareas) and inmarine areas (even far from the estuary) have to beconsidered. Similarly, the management of nature conservationof an estuary has to reflect various scales to cater for the needs ofbiota from outside the immediate system (Borja et al., 2010). Forexample, for wading birds and diadromous fishes there areinfluences associated with the areas they use when not in theestuary; the maintenance of mudflats relies on a sedimentsupply and tidal regime generated elsewhere, and estuarineplants rely on nutrients supplied mainly from the catchment.Hence the health of an estuary has to be measured not only interms of internal features but also external influences, e.g. waterquality issues associated with some developed (industrialisedand urbanised) northern hemisphere estuaries or water quan-tity problems noted for certain southern hemisphere systems(Whitfield and Elliott, 2002). In both hemispheres, the focus ofestuarine health measurements primarily should be on theestuary itself but those outside influences deemed to beimpacting on the estuary also have to be considered (e.g.catchment water balance, upstream pollution events).

(b) Comments/relevance/supportIn both hemispheres, the catchment (including the immediateestuary surrounds) should be a focus for any estuary manage-ment plan but there are differences in our ability to manageterrestrial, freshwater and some estuarine processes (Lotzeet al., 2006; Hering et al., 2010; Borja et al., 2010). There isalso the problem inmany countries where different governmentbodies/management authorities are responsible for themanagement of terrestrial, freshwater, estuarine and marinecomponents (e.g. see Elliott et al., 2006). Getting these differentdepartments/authorities to work together is always difficult andfar more complex than, for example, the management ofa grassland or forest ecosystem.Exogenic events, especially river flooding (whereby the entirecatchment run-off funnels through an estuary) and marinestorm-surge events (once again where estuaries are primaryrecipients of such events), place major pressures on estuaries inboth hemispheres. Sea-level rise has to be accommodated by themanagement (and the ecology) of an estuary (Elliott et al., 2007;FitzGerald et al., 2008) and it has been suggested that thesesystems are adapted to being ‘reset’ from time to time. Indeed,estuarine ecosystemshave to be attuned to being able to respondto radical external influences that transform the habitat at bothregular and irregular intervals. Thus the resilience and resistancein estuaries has to be far greater than other aquatic environ-ments that are not subject to these major external pressures.

Even if an estuary is not dominated by them, it is certainlyreliant on outside events/processes. The resilient nature ofestuaries in both hemispheres means that there is a high degreeof internal ‘control’ and flexibility. For example, this is evidencedby the ability of temporarily closed estuaries in South Africa andAustralia to function very well in the absence (as long as it is notpermanent) of linkages with both the river catchment andmarine environment. Unfortunately, the increasing abstractionof freshwater from river systems in the southern hemisphere isplacing more extreme pressures on the duration of these link-ages, sometimes to the detriment of the estuarine ecosystem(Whitfield and Wooldridge, 1994).Habitat loss is perhaps the major pressure resulting from mostestuarine developments in both the northern and southernhemispheres and this places an increasing pressure on thenatural functioning of estuaries that are already under consid-erable natural stress (Chust et al., 2009). Habitat loss may havebeen temporary, caused by poor water quality from organic andpolluting inputs or water removal, or permanent resulting fromland-claim and infrastructure building (Elliott et al., 2007). Inrecent decades, estuarine habitat creation and restoration hasbeen required to deal with the pressures arising from historicalhabitat loss (Simenstad et al., 2006; Elliott et al., 2007; Lotze,2010; Zedler and Kercher, 2005). In both hemispheres, anyartificial habitat creation is generally at the expense of existingnatural habitat or, in many northern areas, in the form of therecovery of previously destroyed habitats (e.g. managedrealignment/depolderisation).

3.2. Delivery and protection of ecosystem services3.2.1. Paradigm 8

Estuaries provide a wider variety of ecosystem services and anincreased delivery of societal benefits than many other ecosystems.Hence estuaries are one of the most valuable aquatic ecosystemsserving human needs but for this to occur they require functional linkswith the adjoining terrestrial, freshwater and marine systems.

(a) Interpretation/meaningIn the case of the functioning of estuaries in relation to the needsof both natural and social systems, there is a requirement toprotect and enhance the ecosystem services that relate tonatural functioning, while at the same time delivering societalbenefits (Atkins et al., 2011; Zedler and Kercher, 2005). It is alsowidely acknowledged that estuaries are used by society fora wide variety of activities, e.g. transport, harbours, fishing,recreation, human settlements, etc. (O’Higgins et al., 2010). Inturn, given the number of natural processes and linkages withupstream catchment and adjacent terrestrial areas, as well asoffshore and coastal marine areas, then there may be moreecosystem services and societal benefits provided by estuariesthan other aquatic systems (see Atkins et al., 2011 for a table ofecosystem services and societal benefits). Indeed, there hasbeen a change in attitude about freshwater flowing into the seaas being ‘wasted’, to a realisation that the ecosystem services ofcoastal marine areas are closely tied to estuarine inputs(Lamberth et al., 2009; Stoeckl et al., 2011).

(b) Comments/relevance/supportThe distribution of coastal towns, cities and ports in both thenorthern and southern hemispheres indicate a distinct prefer-ence for estuarine localities due to the ecosystem services andsocietal benefits that these ecosystems provide (Pinto et al.,2010; Zedler and Kercher, 2005). These settlements exhibit thefull range of type, from large international harbours, industrialcities, to retirement villages. The real estate value of land on the

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banks of an estuary in both hemispheres is generally muchgreater than equivalent land elsewhere in the same region(Beaumais and Laroutis, 2007) and this alone serves toemphasise the importance of estuaries in the lives of people.

3.3. Concluding comments

It is for the reader to determine whether it is valuable to define,refine and challenge paradigms but we hope that this review hasnot given a too idiosyncratic or personal view. Despite that, theexpectation is that other researchers will add to or modify theparadigms outlined above. Paradigms can be a unifying tool inunderstanding and managing estuaries and we hope that they willprovide a focus on the major issues requiring research attentionworldwide. Although the paradigms discussed here appear inde-pendent of one another and have been given equal weighting, wetake the view that some are more crucial to estuarine ecologicaland management issues than others. We are also aware, as alreadyindicated, of the links between some of the paradigms but feel thatthe specific issues around each one merit a focused discussionwithout ‘dilution’ by related paradigms. The listed paradigms alsoallow us to know the limitations of our science and management,especially if the scientific community is of the opinion that theycannot be tested and defended rigorously. We would especiallywelcome comments and contributions from the wider estuarinecommunity to modify, expand and perhaps even add to those dealtwith in this review.

Acknowledgements

We gratefully acknowledge the many colleagues and authorswho have knowingly or unknowingly contributed to the discus-sions included in this publication. Similarly we are very grateful tothe three anonymous reviewers who provided constructivecomments and suggestions on an earlier version of the paper.

References

Abrantes, K.G., Sheaves, M., 2010. Importance of freshwater flow in terrestrial-aquatic energetic connectivity in intermittently connected estuaries of trop-ical Australia. Marine Biology 157 (9), 2071e2086.

Atkins, J.P., Burdon, D., Elliott, M., Gregory, A.J., 2011. Management of the marineenvironment: integratingecosystemservices andsocietal benefitswith theDPSIRframework in a systems approach. Marine Pollution Bulletin 62 (2), 215e226.

Attrill, M.J., 2002. A testable linear model for diversity trends in estuaries. Journal ofAnimal Ecology 71, 262e269.

Attrill, M.J., Rundle, S.D., 2002. Ecotone or ecocline: ecological boundaries in estu-aries. Estuarine, Coastal and Shelf Science 55, 929e936.

Baird, D., Ulanowicz, R.E., 1993. Comparative study on the trophic structure, cyclingand ecosystem properties of four tidal estuaries. Marine Ecology Progress Series99, 221e237.

Baird, D., Winter, P.E.D., Wendt, G., 1987. The flux of particulate matter througha well mixed estuary. Continental Shelf Research 7, 1399e1403.

Bate, G.C., Whitfield, A.K., Adams, J.B., Huizinga, P., Wooldridge, T.H., 2002. Theimportance of the river-estuary interface zone in estuaries. Water SA 28 (3),271e279.

Beaumais, O., Laroutis, D., 2007. In search of natural resource-based economies: thecase of the Seine Estuary (France). Hydrobiologia 588 (1), 3e11.

Blaber, S.J.M., 1976. The food and feeding ecology of Mugilidae in the St Lucia lakesystem. Biological Journal of the Linnean Society 8, 267e277.

Bodineau, L., Thoumelin, G., Béghin, V., Wartel, M., 1998. Tidal time-scale changes inthe composition of particulate organic matter within the estuarine turbiditymaximum zone in the macrotidal Seine Estuary, France: use of fatty analysisand sterol biomarkers. Estuarine, Coastal and Shelf Science 47 (1), 37e49.

Borja, Á, Elliott, M., Carstensen, J., Heiskanen, A.S., van de Bund, W., 2010. Marinemanagement e towards an integrated implementation of the European marineStrategy framework and the water framework directives. Marine PollutionBulletin 60, 2175e2186.

Borja, Á, Muxika, I., Rodríguez, J.G., 2009. Paradigmatic responses of marine benthiccommunities to different anthropogenic pressures, using M-AMBI, within theEuropean Water Framework Directive. Marine Ecology 30, 214e227.

Boyes, S.J., Elliott, M., 2006. Organic matter and nutrient inputs to the HumberEstuary, England. Marine Pollution Bulletin 53 (1e4), 136e143.

de Brauwere, A., de Brye, B., Blaise, S., Deleersnijder, E., 2011. Residence time,exposure time and connectivity in the Scheldt Estuary. Journal of MarineSystems 84, 85e95.

Bulger, A.J., Hayden, B.P., Monaco, M.E., Nelson, D.M., McCormick-Ray, M.G., 1993.Biologically-based estuarine salinity zones derived from a multivariate analysis.Estuaries 16 (2), 311e322.

Burford, M.A., Revill, A.T., Palmer, T.W., Clementson, L., Robson, B.J., Webster, I.T.,2011. River regulation alters drivers of primary productivity along a river-estuary system. Marine and Freshwater Research 62 (2), 141e151.

Chicharo, L., Chicharo, M.A., 2006. Applying the ecohydrology approach to theGuadiana estuary and coastal areas: lessons learned from dam impactedecosystems. Estuarine, Coastal and Shelf Science 70, 1e2.

Chust, G., Borja, Á, Liria, P., Galparsoro, I., Marcos, M., Caballero, A., Castro, R., 2009.Human impacts overwhelm the effects of sea-level rise on Basque coastal habitats(NSpain)between1954and2004.Estuarine,Coastal andShelfScience84,453e462.

Convention on Biological Diversity (CBD), 2000. Convention on Biological Diversity[Online]. Available: http://www.biodiv.org/default.shtml.

Cyrus, D.P., 1988. Turbidity and other physical factors in Natal estuarine systems.Part 2: estuarine lakes. Journal of the Limnological Society of Southern Africa14, 72e81.

Dürr, H., Laruelle, G., van Kempen, C., Slomp, C., Meybeck, M., Middelkoop, H., 2011.Worldwide typology of nearshore coastal systems: defining the estuarine filterof river inputs to the oceans. Estuaries and Coasts 34, 441e458.

Dauvin, J.C., Ruellet, T., 2009. The estuarine quality paradox: is it possible to definean ecological quality status for specific modified and naturally stressed estua-rine ecosystems? Marine Pollution Bulletin 59 (1e3), 38e47.

Duffy, J.E., Macdonald, K.S., Rhode, J.M., Parker, J.D., 2001. Grazer diversity, func-tional redundancy, and productivity in seagrass beds: an experimental test.Ecology 82 (9), 2417e2434.

Elliott, M., 2011. Marine science and management means tackling exogenicunmanaged pressures and endogenic managed pressures e a numbered guide.Marine Pollution Bulletin 62, 651e655.

Elliott, M., McLusky, D.S., 2002. The need for definitions in understanding estuaries.Estuarine, Coastal and Shelf Science 55 (6), 815e827.

Elliott, M., Quintino, V., 2007. The estuarine quality paradox, environmentalhomeostasis and the difficulty of detecting anthropogenic stress in naturallystressed areas. Marine Pollution Bulletin 54, 640e645.

Elliott, M., Hemingway, K.L., Costello, M.J., Duhamel, S., Hostens, K., Labropoulou, M.,Marshall, S., Winkler, H., 2002. Links between fish and other trophic levels. In:Elliott, M., Hemingway, K.L. (Eds.), Fishes in Estuaries. Blackwell Science,Oxford, pp. 124e216 (Chapter 4).

Elliott, M., Boyes, S.J., Burdon, D., 2006. Integrated marine management andadministration for an island state e the case for a new Marine Agency for theUK. Marine Pollution Bulletin 52 (5), 469e474.

Elliott, M., Burdon, D., Hemingway, K.L., Apitz, S., 2007. Estuarine, coastal andmarine ecosystem restoration: confusing management and science e a revisionof concepts. Estuarine, Coastal and Shelf Science 74, 349e366.

FitzGerald, D.M., Fenster, M.S., Argow, B.A., Buynevich, I.V., 2008. Coastal impactsdue to sea-level rise. Annual Review of Earth and Planetary Science 36,601e647.

Flindt, M.R., Pedersen, C.B., Amos, C.L., Levy, A., Bergamasco, A., Friend, P.L., 2007.Transport, sloughing and settling rates of estuarine macrophytes: mechanismsand ecological implications. Continental Shelf Research 27 (8), 1096e1103.

Folke, C., Carpenter, S., Walker, B., Scheffer, M., Elmqvist, T., Gunderson, L.,Holling, C.S., 2004. Regime shifts, resilience, and biodiversity in ecosystemmanagement. Annual Review of Ecology, Evolution, and Systematics 35,557e581.

Fries, J.S., Noble, R.T., Paerl, W., Characklis, G.W., 2007. Particle suspensions and theirregions of effect in the Neuse River estuary: implications for water qualitymonitoring. Estuaries and Coasts 30 (2), 359e364.

Gómez-Gesteira, M., De Castro, M., Prego, R., 2003. Dependence of the water resi-dence time in Ria of Pontevedra (NW Spain) on the seawater inflow and theriver discharge. Estuarine, Coastal and Shelf Science 58, 567e573.

García-Alonso, J., Greenway, G.M., Munshi, A., Gómez, J.C., Mazik, K., Knight, A.W.,Hardege, J.D., Elliott, M., 2011. Biological responses to contaminants in theHumber Estuary: disentangling complex relationships. Marine EnvironmentalResearch 71 (4), 295e303.

Grange, N., Allanson, B.R., 1995. The influence of freshwater inflow on the nature,amount and distribution of seston in estuaries of the Eastern Cape, South Africa.Estuarine, Coastal and Shelf Science 40, 403e420.

Gray, J.S., Elliott, M., 2009. Ecology of Marine Sediments: Science to Management.OUP, Oxford, 260 pp.

Haines, P.E., Tomlinson, R.B., Thom, B.G., 2006. Morphometric assessment ofintermittently open/closed coastal lagoons in New South Wales, Australia.Estuarine, Coastal and Shelf Science 67, 321e332.

Hering, D., Borja, Á, Carstensen, J., Carvalho, L., Elliott, M., Feld, C.K.,Heiskanen, A.S.K., Johnson, R.K., Moe, J., Pont, D., Solheim, A.L., de Bund, W.V.,2010. The European Water Framework Directive at the age of 10: a criticalreview of the achievements with recommendations for the future. Science ofthe Total Environment 408, 4007e4019.

Hilmer, T., Bate, G.C., 1990. Covariance analysis of chlorophyll distribution in theSundays River estuary. Southern African Journal of Aquatic Sciences 16, 37e59.

Howe, E.R., Simenstad, C.A., 2011. Isotopic determination of food web origins andestuarine ancient wetlands of the San Francisco Bay and delta. Estuaries andCoasts 34 (3), 597e617.

M. Elliott, A.K. Whitfield / Estuarine, Coastal and Shelf Science 94 (2011) 306e314314

Hughes, T.P., Bellwood, D.R., Folke, C., Steneck, R.S., Wilson, J., 2005. New paradigmsfor supporting the resilience of marine ecosystems. Trends in Ecology &Evolution 20, 380e386.

Hume, T.M., Snelder, T., Weatherhead, M., Liefting, R., 2007. A controlling factorapproach to estuary classification. Ocean and Coastal Management 50,905e929.

Jerling, H.L., Wooldridge, T.H., 1991. Population dynamics and estimates ofproduction for the calanoid copepod Pseudodiaptomus hessei in a warmtemperate estuary. Estuarine, Coastal and Shelf Science 33, 121e135.

de Jonge, V.N., Van Beusekom, J.E., 1995. Wind and tide-induced resuspension ofsediment and microphytobenthos from tidal flats in the Ems Estuary.Limnology and Oceanography 40, 766e778.

de Jonge, V.N., Elliott, M., 2002. Causes, historical development, effects and futurechallenges of a common environmental problem: eutrophication. Hydro-biologia 475/476, 1e19.

Kremer, J.N., Vaudrey, J.M.P., Ullman, D.S., Bergondo, D.L., LaSota, N., Kincaid, C.,Codiga, D.L., Brush, M.J., 2010. Simulating property exchange in estuarineecosystem models at ecologically appropriate scales. Ecological Modelling 221,1080e1088.

Kuhn, T.S., 1970. The Structure of Scientific Revolutions, second ed. University ofChicago Press, Chicago, 222 pp.

Kuzyk, Z.A., Macdonald, R.W., Granskog, M., Scharien, R.K., Galley, R.J., Michel, C.,Barber, D., Stern, G., 2008. Sea ice, hydrological, and biological processes in theChurchill River estuary region, Hudson Bay. Estuarine, Coastal and Shelf Science77 (3), 369e384.

Lamberth, S.J., Drapeau, L., Branch, G.M., 2009. The effects of altered freshwaterinflows on catch rates of non-estuarine-dependent fish in a multispeciesnearshore linefishery. Estuarine, Coastal and Shelf Science 84 (4), 527e538.

Lin, H.-J., Dai, X.-X., Shao, K.-T., Su, H.-M., Lo, W.-T., Hsieh, H.-L., Fang, L.-S., Hung, J.-J., 2006. Trophic structure and functioning in a eutrophic and poorly flushedlagoon in southwestern Taiwan. Marine Environmental Research 62 (1), 61e82.

Loreau, M., Naeem, S., Inchausti, P., 2002. Biodiversity and Ecosystem Functioning:Synthesis and Perspectives. Oxford University Press, Oxford.

Lotze, H.K., 2010. Historical reconstruction of human-induced changes in U.S.Estuaries. Oceanography and Marine Biology: an Annual Review 48, 267e338.

Lotze, H.K., Lenihan, H.S., Bourque, B.J., Bradbury, R.H., Cooke, R.G., Kay, M.C.,Kidwell, S.M., Kirby, M.X., Peterson, C.H., Jackson, J.B.C., 2006. Depletion,degradation, and recovery potential of estuaries and coastal seas. Science 312,1806e1809.

Marais, J.F.K., 1982. The effects of river flooding on the fish populations of twoeastern Cape estuaries. South African Journal of Zoology 17, 96e104.

McLusky, D.S., Elliott, M., 2004. The Estuarine Ecosystem; Ecology, Threats andManagement, third ed. Oxford University Press, Oxford, 216 pp.

McLusky, D.S., Elliott, M., 2007. Transitional waters: a new approach, semantics orjust muddying the waters? Estuarine, Coastal and Shelf Science 71 (3e4),359e363.

McLusky, D.S., Hull, S.C., Elliott, M., 1993. Variations in the intertidal and subtidalmacrofauna and sediments along a salinity gradient in the Upper Forth estuary.Netherlands Journal of Aquatic Ecology 27, 101e109.

Milliman, J.D., 2001. Delivery and fate of fluvial water and sediment to the sea:a marine geologist’s view of European rivers. Scientia Marina 65, 121e132.

Milliman, J.D., Farnsworth, K.L., Jones, P.D., Xu, K.H., Smith, L.C., 2008. Climatic andanthropogenic factors affecting river discharge to the global ocean, 1951e2000.Global and Planetary Change 62, 187e194.

Monsen, N.E., Cloern, J.E., Lucas, L.V., Monismith, S.G., 2002. A comment on the useof flushing time, residence time, and age as transport time scales. Limnologyand Oceanography 47, 1545e1553.

Ter Morshuizen, L.D., Whitfield, A.K., Paterson, A.W., 1996. Influence of freshwaterflow regime on fish assemblages in the Great Fish River and estuary. SouthernAfrican Journal of Aquatic Sciences 22, 52e61.

Neto, J.M., Flindt, M.R., Marques, J.C., Pardal, M.A., 2008. Modelling nutrient massbalance in a temperate meso-tidal estuary: implications for management.Estuarine, Coastal and Shelf Science 76, 175e185.

Nicolas, D., Lobray, J., Lepage, M., Sautour, B., Le Pape, O., Cabral, H., Uriarte, A.,Boët, P., 2010. Fish under influence: a macroecological analysis of relationsbetween fish species richness and environmental gradients among Europeantidal estuaries. Estuarine, Coastal and Shelf Science 86 (1), 137e147.

O’Higgins, T.G., Ferraro, S.P., Dantin, D.D., Jordan, S.J., Chintala, M.M., 2010. Habitatscale mapping of fisheries ecosystem service values in estuaries. Ecology andSociety 15, 7 [online] URL. http://www.ecologyandsociety.org/vol15/iss14/art17.

Odum, E., 2002. Tidal Marshes as outwelling/pulsing systems. Concepts andControversies in tidal Marsh ecology (1), 3e7. doi:10.1007/0-306-47534-0_1.

Odum, W.E., Odum, E.P., Odum, H.T., 1995. Nature’s pulsing paradigm. Estuaries 18(4), 547e555.

OECD, 1993. Organisation for Economic Co-operation and Development (OECD)Core Set of Indicators for Environmental Performance Reviews. In: OECDEnvironment Monographs No. 83 Paris.

Pinto, R., Patricio, J., Neto, J.M., Salas, F., Marques, J.C., 2010. Assessing estuarinequality under the ecosystem services scope: ecological and socio-economicaspects. Ecological Complexity 7, 389e402.

Potter, I.C., Chuwen, B.M., Hoeksema, S.D., Elliott, M., 2010. The concept of anestuary: a definition that incorporates systems which can become closed to theocean and hypersaline. Estuarine, Coastal & Shelf Science 87, 497e500.

Remane, A., 1934. Die Brackwasserfauna. Verhein Deutsche Zoologische Geselschaft36, 34e74.

Remane, A., Schlieper, C., 1971. Biology of Brackish Water. E. Schweiserbart’scheVerlagsbuchhandlung, Stuttgart.

Richardson, N., Gordon, A.K., Muller, W.J., Whitfield, A.K., 2011. A Weight-of-evidence Approach to Determine Estuarine Fish Health Using Indicators fromMultiple Levels of Biological Organization. Aquatic Conservation: Marine andFreshwater Ecosystems 21, 423e432.

Saiz-Salinas, J.I., González-Oreja, J.A., 2000. Stress in estuarine communities:lessons from the highly impacted Bilbao estuary (Spain). Journal of AquaticEcosystem Stress and Recovery 7 (1), 43e55.

Simenstad, C., Reed, D., Ford, M., 2006. When is restoration not? incorporatinglandscape-scale processes to restore self-sustaining ecosystems in coastalwetland restoration. Ecological Engineering 26, 27e39.

Stoeckl, N., Hicks, C.C., Mills, M., Fabricius, K., Esperon, M., Kroon, F., Kaur, F.,Costanza, R., 2011. The economic value of ecosystem services in the GreatBarrier Reef: our state of knowledge. Annals of the New York Academy ofSciences 1219 (1), 113e133.

Taljaard, S., van Niekerk, L., Joubert, W., 2009. Extension of a qualitative model onnutrient cycling and transformation to include microtidal estuaries on wave-dominated coasts: southern hemisphere perspective. Estuarine, Coastal andShelf Science 85, 407e421.

Telesh, I.V., Schubert, H., Skarlato, O., 2011. Revisiting Remane’s concept: evidencefor a high plankton diversity and a protistan species maximum in the hor-ohalinicum of the Baltic Sea. Marine Ecology Progress Series 412, 1e11.

Uncles, R.J., 2010. Physical properties and processes in the Bristol Channel andSevern estuary. Marine Pollution Bulletin 61, 5e20.

Vaudrey, J.M.P., Kremer, J.N., Branco, B.F., Short, F.T., 2010. Eelgrass recovery afternutrient enrichment removal. Aquatic Botany 93 (4), 237e243.

Whitfield, A.K., 1984. The effects of prolonged aquatic macrophyte senescence onthe biology of the dominant fish species in a southern African coastal lake.Estuarine, Coastal and Shelf Science 18, 315e329.

Whitfield, A.K., 1988. The role of tides in redistributing macrodetrital aggregateswithin the Swartvlei estuary. Estuaries 11, 152e159.

Whitfield, A.K., 1990. Life-history styles of fishes in South African estuaries. Envi-ronmental Biology of Fishes 28, 295e308.

Whitfield, A.K., 2005. Langebaan e A new type of estuary? African Journal ofAquatic Science 30 (2), 207e209.

Whitfield, A.K., Elliott, M., 2002. Fishes as indicators of environmental andecological changes within estuaries e a review of progress and some sugges-tions for the future. Journal of Fish Biology 61 (Suppl. A), 229e250.

Whitfield, A.K., Elliott, M., in press. Ecosystem and biotic classifications of estuariesand coasts, (Chapter 1) 8; In: Wolanski, E., McLusky, D.S. (Eds), Treatise onEstuaries and Coasts, Elsevier, Amsterdam.

Whitfield, A.K., Harrison, T.D., 2003. River flow and fish abundance in a SouthAfrican estuary. Journal of Fish Biology 62, 1467e1472.

Whitfield, A.K., Wooldridge, T.H., 1994. Changes in freshwater supplies to southernAfrican estuaries: some theoretical and practical considerations. In: Dyer, K.R.,Orth, R.J. (Eds.), Changes in Fluxes in Estuaries: Implications from Science toManagement. Olsen & Olsen, Fredensborg, Denmark, pp. 41e50.

Whitfield, A.K., Adams, J.B., Bate, G.C., Bezuidenhout, K., Bornman, T.G., Cowley, P.D.,Froneman, P.W., Gama, P.T., James, N.C., Mackenzie, B., Riddin, T., Snow, G.C.,Strydom, N.A., Taljaard, S., Terörde, A.I., Theron, A.K., Turpie, J.K., van Niekerk, L.,Vorwerk, P.D., Wooldridge, T.H., 2008. A multidisciplinary study of a small,temporarily open/closed South African estuary, with particular emphasis on theinfluence of mouth state on the ecology of the system. African Journal of MarineScience 30 (3), 453e473.

Wolanski, E., 2007. Estuarine Ecohydrology. Elsevier, Amsterdam, 168 pp.Wolanski, E., Boorman, L.A., Chicharo, L., Langlois-Saliou, E., Lara, R., Plater, A.J.,

Uncles, R.J., Zalewski, M., 2004. Ecohydrology as a new tool for sustainablemanagement of estuaries and coastal waters. Wetlands Management andEcology 12, 235e276.

Zedler, J.B., Kercher, S., 2005. Wetland resources: status, ecosystem services,degradation, and restorability. Annual Review of Environment and Resources30, 39e74.