Challenging paradigms in estuarine ecology and management

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

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Challenging paradigms in estuarine ecology and management M. Elliott a, *, A.K. Whitfield b a b

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

a r t i c l e i n f o

a b s t r a c t

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

For many years, estuarine science has been the ‘poor relation’ in aquatic research e freshwater scientists ignored estuaries as they tended to get confused by salt and tides, and marine scientists were more preoccupied by large open systems. Estuaries were merely regarded by each group as either river mouths or 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 has led to paradigms being generated to summarise estuarine structure and functioning and which relate to both the natural science and management of these systems. This paper defines, details and affirms these paradigms that can be grouped into those covering firstly the science (definitions, scales, linkages, productivity, tolerances and variability) and secondly the management (pressures, valuation, health and services) of estuaries. The more ‘science’ orientated paradigms incorporate the development and types of ecotones, the nature of stressed and variable systems (with specific reference to resilience and redundancy), the relationship between generalists and specialists produced by environmental tolerance, the relevance of scale in relation to functioning and connectivity, the sources of production and degree of productivity, the biodiversity-ecosystem functioning and the stress-subsidy debates. The more ‘management’ targeted paradigms include the development and effects of exogenic unmanaged pressures 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 of ecosystem services and societal benefits. Ó 2011 Elsevier Ltd. All rights reserved.

Keywords: estuaries paradigms ecology management

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

* Corresponding author. E-mail addresses: [email protected] (M. Elliott), a.whitfi[email protected] (A.K. Whitfield). 0272-7714/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2011.06.016

This paper aims to present a set of paradigms relating to both northern and southern hemisphere estuaries. Here the term paradigm is used to mean a set of concepts or accepted philosophies that define a field of science which has been developed over the history of a field, but which are amenable to testing via the scientific method using hypothesis generation. Kuhn (1970) considers that a scientific paradigm can cover concepts and observations, questions and hypotheses and the interpretation of field, laboratory and modelling observations, measurements and outcomes. Hence there must be the ability to prove or disprove the paradigms or to test for deviations from what is accepted. Here we take the view that paradigms do not have to be mutually exclusive and they should comprise a set of unifying concepts central to the science and management. It is widely acknowledged that paradigms can develop from a comment in a published paper (with all its caveats) to become a hard fact (without caveats) by the time the ‘fact’ has been put into a book. The ‘fact’ then keeps being repeated, without it being tested rigorously, and is thus reinforced as a ‘fact’ within the scientific community. Hence there is a need to reject, reaffirm or test current paradigms in estuarine ecology and management. Furthermore, there is the need

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to determine paradoxes within or between paradigms and also to determine whether a paradigm holds for a given geographical area, an estuary type or is more widely applicable. By definition, a paradigm should hold across the discipline, and hence paradigms need to be tested and rejected when found not to hold true. There is the constant need to review paradigms in the light of new information and understanding, and there is also a need to acknowledge that they sometimes challenge our view of the topic and may even give new directions for future research. We take the view that a paradigm should stand up to scrutiny and if it fails that test then it should be discarded. We also contend that paradigms are challenging because they are generally structured around some fundamental aspect of science (often ecological functioning in the case of estuaries). The paradigms outlined below have been gathered by our reading, refereeing, editing and writing of estuarine papers, chapters and books over many decades. While writing this review, we started with 35 statements and refined that to 20 after deciding that some applied to estuaries in one part of the world but not another. From that second iteration it was decided to merge and refine these 20 to the final set of eight given here. Those final paradigms were then presented at the April 2011 international symposium of ECSA/SAMSS held in Grahamstown, South Africa, and then refined further using discussions and feedback. The proposed paradigms of course need supporting and, while references are given here where possible, this is occasionally difficult for those paradigms which by their very nature tend to be obscure in terms of actual origin. This contrasts to formulae, indices and laws which are usually linked to a particular published paper. Accordingly, here we detail, expand, propose, define, comment and challenge and/or affirm the selected paradigms. Other estuarine scientists may disagree or have additional paradigms but this preliminary list is presented to stimulate debate and discussion. 2. Natural science-based paradigms 2.1. Definitions, scales, ecotones and linkages 2.1.1. Paradigm 1 An estuary is an ecosystem in its own right but cannot function indefinitely on its own in isolation and that it depends largely on other ecosystems, possibly more so than do other ecosystems. (a) Interpretation/meaning An ecosystem can be defined as: ‘a dynamic complex of plant, animal and micro-organism communities and their non-living environment interacting as a functional unit’ (CBD, 2000). Most estuarine characteristics relate to connections and connectivity with freshwater and marine areas; therefore for a system to be an estuary it has, by definition, to depend on other systems (Dürr et al., 2011). Of course, very few large ecosystems are selfcontained and they all have some degree of interlinking. No natural ecosystem is completely closed (e.g. the rainfall cycle affects just about every ecosystem, it is global and not closed) but on an open/closed scale, estuaries are mostly very ‘open’ systems given their strong connectivity with both the riverine and marine environments (Gómez-Gesteira et al., 2003; Kremer et al., 2010). While all ecosystems are linked to the atmosphere, no others have simultaneous connectivity to freshwater catchment and terrestrial influences, the atmosphere and marine systems e thus in many respects estuaries could be regarded as multi-interface systems, i.e. ecosystems with multiple major influences and boundaries. Whilst they are open, however, they are ecosystems with their own specific characteristics and exist because of their almost continuous links with rivers or the sea or both. However, for those estuaries that are occasionally closed by sand bars

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because of low river flows, the available evidence suggests that an intermittent system will continue to function as an estuary as long as it opens on occasions (Whitfield et al., 2008). (b) Comments/relevance/support We contend that an ecosystem can be defined by its paradigms. There has long been a debate on what is an estuary, partly because there is greater variability in the structure and nature of estuaries around the world than there is for example between tropical forests around the world e hence the ongoing debate around what is an estuary (Elliott and McLusky, 2002; Whitfield, 2005). Northern hemisphere scientists approached the definition of an estuary based on high freshwater input systems (see Elliott and McLusky, 2002, and references therein for a discussion of definitions of estuaries), whereas southern hemisphere scientists have to deal with a variety of systems, many of which have very limited riverine inputs associated with arid climates (Potter et al., 2010). Arguably the largest problem confronting those systems is the lack of freshwater inputs which may cover medium or long periods, hence giving rise to closed systems and/or hypersaline areas. It is emphasised that while arid areas occur in the northern regions, and thus create particular types of estuaries which behave similarly to arid zone estuaries worldwide, these are more common in the south. In addition, the proportionally larger number of intermittently open estuaries in the southern hemisphere also tends to lead to a divergence between the north and south on what constitutes a typical estuary. The microtidal nature of many southern hemisphere coasts is also very different to the macrotidal characteristics of many northern hemisphere coasts (where most estuarine research has been conducted). Thus the significant marine influence on large North American and European estuaries overshadows the more limited marine influence on southern hemisphere estuaries. In contrast to many southern systems, many northern ones are usually open or at most only partly closed by ebb-tide deltas and/ or barrier islands; hence they tend to have constant links between sea and freshwaters, whereas many southern systems do not, especially in southern Africa and Australia. Evidence from temporarily closed estuaries in the southern hemisphere suggests that estuaries can function in isolation for many years (during prolonged droughts) and that they can ‘bounce back’ very quickly once the connectivity with marine and freshwater systems is restored. For example, the East Kleinemonde Estuary, continuously monitored since the early 1990s (Whitfield et al., 2008), is currently experiencing a more than 3-year effective closed phase, yet both marine and estuarine fish species appear to be maintaining their populations and ecological balance very well. 2.1.2. Paradigm 2 As ecosystems, estuaries are more influenced by scale than any other aquatic system; their essence is in the connectivity across the various scales and within the water body they are characterised by one or more ecotones. (a) Interpretation/meaning Estuaries, as with all ecosystems, respond to processes operating at different scales but this paradigm suggests that for estuaries the scales range from internal (within estuary), to local (between estuaries, between estuary-river, between estuarysea), to larger biogeographical scales. For example, the latter includes the links between polar breeding grounds for temperate estuarine wading birds and the migrations from the open ocean to coastal regions for eels.

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If an ecotone is defined (Attrill and Rundle, 2002) as being a transition/gradient between two systems, then estuaries can be regarded as having several ecotones e into the estuary from adjacent freshwater catchments, out of the estuary to the marine/coastal area, laterally from the supratidal region into the littoral margins, vertically from the air interface into the surface waters, from the water column into the estuary bed, and with depth/stratification throughout the water column. The relative size (spatial dimension), influence and temporal presence of each of these ecotones varies with locality and type of estuary. While classically an ecotone would be expected to have an increased biodiversity due to the mixing of two adjacent systems, either this does not appear to occur in estuarine ecotones or it has not been documented (Attrill, 2002). (b) Comments/relevance/support The scales of both the estuary size and the catchment area of many northern hemisphere estuarine systems appear to be much larger and cover a wider area than those in most southern hemisphere situations. This may be related to the larger riverine discharges (on average) into the northern hemisphere estuaries which accentuate the size of the transitional waters at both the head and mouth regions of these systems (Milliman, 2001). The scales of temperature variation in estuaries are also much larger in the northern hemisphere because the continents where most studies have been conducted are at higher latitudes than equivalent systems in the southern hemisphere. For example, the Rhine is a large estuary with an international catchment whose organisms are dependent on an area from the poles (for the overwintering wading birds) to the western Atlantic/Sargasso Sea (for eels). Although some of the larger African temperate estuaries in the southern hemisphere host palaeoarctic migrant bird species from Europe and Asia, and anguillid eels from as far a field as Madagascar, none of these systems freeze over in winter as occurs in some northern temperate estuaries (Kuzyk et al., 2008). The importance and presence of ecotones may relate to the size of the estuaries and their catchment inputs. Thus many smaller southern 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) whereas the larger and deeper northern estuaries with large perennial riverine inflows show all the characteristics and ecotones mentioned 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 head may migrate further down into the estuary under high flow conditions) they still are preserved spatially. Closed-mouth estuaries lose their longitudinal ecotones (estuarine-marine and estuarine-freshwater) for the period that they are closed, which may be seasonally or for up to several years during extended droughts. Well-mixed estuaries conceivably will have lost their lateral and vertical ecotones and these are more likely to occur in small shallow temporarily open/closed southern hemisphere systems (Whitfield et al., 2008). In addition, for some small temporarily closed estuaries there is sometimes no ecotone between the freshwater environment and marine environment and estuary due to a temporary cessation of river flow during the dry season (Taljaard et al., 2009; Potter et al., 2010). For open estuaries, the presence and influence of ecotones may vary daily with diurnal tides, on a spring-neap cycle, seasonally or interannually. Hence the paradigm suggests that while ecotones do not have to be present continually, they are central to overall estuarine functioning.

2.2. Hydromorphological and organic functioning 2.2.1. Paradigm 3 Hydromorphology is the key to understanding estuarine functioning but these systems are always influenced by salinity (and the resulting density/buoyancy currents) as a primary environmental driver. (a) Interpretation/meaning Hydromorphology is regarded and can be interpreted as representing the links between the sediments and suspended sediment, water movements and tidal balance, all of which influence the estuarine biota and are superimposed on the underlying geology/geomorphology of the system (Gray and Elliott, 2009; Nicolas et al., 2010). Hydromorphology will be the primary determinant for the residence time of water within an estuary and this will have a major impact on the ecological functioning 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 suggests everything else is secondary) but most estuary-associated species are highly euryhaline (see also Bulger et al., 1993). River flow, especially in the context of estuarine morphology, is also of high importance and a key component in the understanding of hydromorphology (Gómez-Gesteira et al., 2003). Based on the hydromorphology, the estuarine characteristics and thus pressures on the biota are therefore shaped by the relative influence of the tides and river inputs, the creation of a Turbidity Maximum Zone (especially in northern hemisphere systems), and in turn poor water column light conditions preventing/limiting primary production (Burford et al., 2011). The density/buoyancy driven currents produced by water bodies of different salinity (and temperature) interacting appear to be central to the hydrodynamic functioning of all estuaries although they do have differing strengths of influence (Wolanski et al., 2004; Uncles, 2010). Furthermore, the net result of the tidal and freshwater influences creates the flushing rate and its corollary the residence time (Monsen et al., 2002), both of which influence in turn the salinity, the ability to retain nutrients, the dispersal of certain stages of benthic organisms and plankton and the wider connectivity between systems (de Brauwere et al., 2011). (b) Comments/relevance/support Hydromorphology is a major driver of estuarine ecosystem functioning in that it can lead to both changed salinity conditions and/or the physical removal of organisms. There are many examples of strong river flow driving euryhaline marine fishes out of more linear estuaries (Whitfield and Harrison, 2003), even though they can survive in freshwater or oligohaline waters for prolonged periods (Ter Morshuizen et al., 1996). This may suggest a hierarchy of the influence of physical factors and that the hydromorphology influence may be more of a global paradigm than that of salinity for certain systems (Marais, 1982). The hydromorphology will influence sediment inputs from riverine systems, as well as tidal pulsing and the creation of high turbidity areas in many estuaries. This in turn will affect the water column primary productivity and perhaps the key question here is whether turbidity is more important in structuring estuarine assemblages than light, or whether the two must be dealt with together. The level of turbidity has the potential to determine whether a system becomes eutrophic by retaining nutrients or whether it merely exports nutrients to the receiving coastal waters (de Jonge and Elliott, 2002). Even highly turbid estuaries such as St Lucia (South Africa), that are severely light limited for much of the time (Cyrus, 1988), are biologically

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diverse and productive ecosystems. Some northern hemisphere estuaries also have high levels of suspended solids and/or phytoplankton, with tidal resuspension of microphytobenthos and benthic organic material also contributing to elevated turbidity levels (Bodineau et al., 1998; Fries et al., 2007). For example, the Humber Estuary, eastern England, consistently has turbidity levels exceeding 5 g l 1 thus influencing its water column productivity (Boyes and Elliott, 2006). In shallow estuarine systems (e.g. <5 m depth), water column mixing is often wind-driven and therefore phytoplankton and microphytobenthos are brought to the water surface regularly due to vertical circulation (Grange and Allanson, 1995; de Jonge and Van Beusekom, 1995). In general, estuaries in both the northern and southern hemispheres are more turbid than clear, hence the lack of colour in invertebrates, fishes, etc. in both hemispheres. From a light perspective, the functioning of most temperate estuaries during the winter is not affected as there are sufficiently high light intensities for photosynthesis in the water column and by epiphytes to occur. In addition, as discussed below, the detrital inputs associated with estuaries mean that the annual production cycle is more dampened and less pronounced than in open sea systems (i.e. spring and autumn phytoplankton blooms are not as pronounced in estuaries but detritus is present in large quantities throughout the year for consumers). 2.2.2. Paradigm 4 Although estuaries behave as sources and sinks for nutrients and organic matter, in most systems allochthonous organic inputs dominate over autochthonous organic production. (a) Interpretation/meaning While estuaries have an abundance of autochthonous producing fringing areas (e.g. reedbeds, seagrass meadows, mangroves and saltmarshes), they also receive large amounts of organic material from riverine primary producers, the sea and even from anthropogenic waste (Abrantes and Sheaves, 2010; Howe and Simenstad, 2011). Allochthonous organic matter and nutrients flow into an estuary mainly from the catchment and adjacent wetlands and may be retained there, thus fuelling a detritusbased system. Once in the system, depending on its flushing characteristics, some of the materials may also flow to the adjacent marine area via the estuarine plume or be redistributed within the estuary by tidal action (Baird et al., 1987; Whitfield, 1988). The ecomorphometry of an estuary (regarded here as the physical shape of the estuary but influenced and modified by organisms and their influence on their habitats) is likely to be the main determinant of the amount of authochthonous and allochthonous inputs retained within a system (Lin et al., 2006). Channellike estuaries are likely to be poor sinks for nutrients and organic matter whereas lacustrine, segmented or compartmentalised estuaries are more likely to retain much of these products, even under high river flow conditions. It is important to note that the delivery of nutrients and organics to any estuary from a river, as well as exchanges between the estuary and marine environment, does not usually occur at a constant rate but are pulsed (Odum et al., 1995) such that most may be delivered in a small number of high flow events; this has been termed the pulsing paradigm by Odum (2002). (b) Comments/relevance/support Systems in both the northern and southern hemispheres act as ‘detritus traps’ of both allochthonous and autochthonous production. Although the proportion/balance between the two

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sources will vary on both a temporal and spatial scale, this phenomenon occurs in estuarine systems in both hemispheres (Baird and Ulanowicz, 1993). Southern hemisphere estuaries that have a closed-mouth phase are the ultimate sink and, when they burst open, usually following river flooding, they are then a primary source of large quantities of nutrients and organic matter to the adjacent sea area. This process is particularly important in seas with low nutrient levels (e.g. the east coast of southern Africa), but not where seas have high nutrient levels (e.g. the west coast of southern Africa). Many northern hemisphere estuaries are large sources and sinks for nutrients and organic matter by virtue of their size, high riverine inputs and broad/deep mouth regions (Boyes and Elliott, 2006). Estuaries entering the Mediterranean are important sources of nutrients for those often oligotrophic areas, whereas estuaries entering the north-west Atlantic may not necessarily have the same impact. Whilst all estuaries are sources of organic matter to adjacent coastal zones, there are differences between a constant input to the sea with uniform flows, and those systems where pulsed inputs can transfer a major nutrient and organic input in a single spate. Therefore the source-sink magnitudes are linked to hydromorphology constraints and forcing factors, e.g. wet climatic periods due to the North Atlantic Oscillation or El Niño/ La Niña can both deliver large amounts of catchment nutrients into estuaries and the adjacent ocean, as well as flush accumulated nutrients and organic matter from these systems. The ability of an estuary to convert nutrients to organic matter depends primarily on the residence time and light regime, e.g. a short residence time (caused by a high tidal range and/or freshwater flushing) and high turbidity will result in nutrients entering the system being exported to the adjacent coast before having the opportunity to be used by plants within the estuary. Conversely, an increased residence time favours autochthonous production and can even result in phytoplankton or flagellate blooms developing within an estuary (Hilmer and Bate, 1990). 2.3. Variability, resilience and redundancy 2.3.1. Paradigm 5 Estuaries are physico-chemically more variable than other aquatic systems but estuarine communities are less diverse taxonomically and the individuals are more physiologically adapted to environmental variability than equivalent organisms in other aquatic systems. (a) Interpretation/meaning Salinity and temperature can change greatly over tidal cycles; this is especially the case in temperate northern estuaries but also for southern ones over very long cycles of opening and closing. This high variability results in estuaries being biologically much less diverse than equivalent aquatic ecosystems elsewhere (e.g. coral reefs). However, those organisms living in estuaries have an inherent ecological tolerance of environmental variability, such that these systems can absorb natural and anthropogenic stress more effectively than other aquatic ecosystems. Consequently estuaries and estuarine organisms have a high resilience to change when compared to the situation in more stable aquatic environments. The strong concurrent spatial and temporal gradients and variability in salinity (and therefore osmotic pressure on the organisms) and temperature, and in some systems pH and Eh (redox potential changes), thus produce a challenging set of physico-chemical variables which leads to a unique aquatic chemistry. Furthermore, this then results in their unique ecology. The high degree of variability in estuarine systems has dictated that organisms living in these areas have a greater

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ability to tolerate and recover from stress (as adverse environmental conditions) at the individual, population and community levels. Redundancy refers to an ability to remove elements and still function, or to have spare capacity, whereas resilience signifies the ability to recover from stress-induced change (Elliott et al., 2007; see also Folke et al., 2004, for a discussion of the concepts). Although estuarine biota are highly resilient to physico-chemical changes to their environment, there is a limited pool of species from which to draw should extreme conditions result in the loss of only a few species from the system, i.e. the degree of inter-specific redundancy in estuaries is relatively low when compared to that found in many marine systems (Hughes et al., 2005). However, the large populations of the relatively few species present may mean that intra-specific redundancy is high. Ecological redundancy in estuaries has yet to be tested in relation to the removal of organisms within a population, of species within a community, or of communities within habitats. Studies of these aspects are rare (Duffy et al., 2001) but indications are that redundancy may differ between biotic groups, especially the presence or absence of possible replacement species when key taxa are eliminated. For example, in South African estuaries there are usually only one or two submerged macrophyte species that can survive particular estuarine conditions. The loss of just one of these species from an estuary often results in the disappearance of this type of habitat from the system altogether (Whitfield, 1984) (i.e. there is no redundancy). As estuaries in general may be species-poor, caused primarily by the high physico-chemical variability, the risk of a lack of redundancy needs to be carefully assessed when placing additional anthropogenic pressures on these systems. (b) Comments/relevance/support Estuaries in both hemispheres have spatial and temporal variability, related to river flows, tidal inputs, sediment balance and erosion-deposition cycles. Organisms in the intertidal and supratidal zone of coastal waters also have to withstand variability (of wave action, sediment instability, temporary desiccation, high and low salinity due to evaporation and rainfall, etc) but this variability is more ‘predictable’ than that occurring in estuaries. Hence estuaries may be regarded paradoxically as being ‘constantly variable’ rather than having a consistent variability! In order to withstand that variability, euryoecious estuarine organisms should be considered as being more diverse physiologically than stenoecious organisms in the adjacent marine areas. Given the fact that there is already a relatively low species diversity when compared to all the freshwater and marine species adjacent to the estuary, the loss of only a few species can have a major impact on entire food chains, e.g. the collapse of Zostera or Ruppia beds in an estuary usually results in bare sediments because there are no other estuarine aquatic macrophyte species to replace them. Conversely the loss of seagrasses under eutrophic conditions often leads to replacement by opportunistic green algae (Vaudrey et al., 2010). This type of succession breakdown would not happen in a terrestrial environment because other species would immediately replace those lost. The superabundance (hence conferring a large amount of trophic redundancy) of detritus in estuaries in both hemispheres is emphasised by Blaber (1976) who showed that the mugilid fishes (detritivores) are all targeting detritus (particulate organic matter) as a primary food source, with little dietary separation between the species. One of the hypotheses arising

from that work was that there is a possible excess supply of detritus to estuarine systems, thus minimising competitive interactions between detritivores. The superabundance of detritus leads to a general acceptance that estuaries are ‘rich’ in detritus (Flindt et al., 2007) and that many animals in estuaries are detritivores. Hence the dominance by detritivores, comprising both invertebrates and fishes, is an underlying feature of most estuaries and invertebrate detritivores covers bivalve suspension feeders and epibenthic, benthic and infaunal detrital consumers (McLusky and Elliott, 2004). In turbid northern estuaries, suspension feeders are limited by both a poor phytoplankton food resource and the energetic deficit caused by excessive gill cleaning. Accordingly, in many of these estuaries the foodwebs have a central dominant detritivore, either epibenthic crustaceans or infaunal sediment feeders, and higher predators (fishes and birds) which are generalists in that they take any prey they encounter (Elliott et al., 2002). 2.4. Diversity, tolerances, stress, productivity 2.4.1. Paradigm 6 Estuaries are systems with low diversity/high biomass/high abundance and their ecological components show a diversity minimum in the oligohaline region which can be explained by the stress-subsidy concept where tolerant organisms thrive but non-tolerant organisms are absent. (a) Interpretation/meaning The diversity of many components is at a minimum in the oligohaline area of estuaries (Remane and Schlieper, 1971) where there are few species because of the stressful conditions but those that can survive have a subsidy and create large populations. The resulting high biomass in this region is related to a large production and inputs of organic matter and nutrients, with the large populations possibly also resulting from a lack of inter-specific competition. The tolerance range of organisms limit which species can occur in a water body, hence there is a lower diversity in estuaries than in rivers or at sea. Although diversity is related to the size of an area and the number of niches, the paradox here is that estuarine areas are physico-chemically variable, hence there are different water-column niches but only tolerant species can cope with the variability. This results in low diversity (taxonomically) but considerable production, rapid growth rates, etc., by species tolerant of these conditions. Although as yet it needs to be tested, estuaries may show the converse of the Biodiversity-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 texts emphasise that estuaries are stressful systems for aquatic organisms (e.g. Saiz-Salinas and González-Oreja, 2000; McLusky and Elliott, 2004). However, there is a paradox here in that they are only stressed systems for organisms which cannot tolerate the conditions and thus usually may not survive and that organisms adapted to estuarine conditions therefore have ideal conditions for survival and growth. Perhaps the central feature of estuarine ecology is that these ecosystems are only stressful for those organisms which are not well-adapted for these conditions; hence for a stenohaline species a euryhaline area is likely to create physiological stress and thus they are likely to be absent. Furthermore, because of reduced inter-specific competition, any organisms tolerant of estuarine conditions have a subsidy and will thrive in these systems (although intraspecific competition may become more important than interspecific competition).

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The estuarine biota comprises more generalists than specialists, in terms of physiological tolerances and feeding strategies, and they tend to be dominated by r-strategists and T-strategists rather than k-strategists (Gray and Elliott, 2009). It would appear that particularly for the zooplankton, zoobenthos and algae, and especially in the upper reaches (the main salinity transition areas) most species are r-strategists, i.e. short lived, high turnover, small bodied, fast colonisers; characteristics related not only to the physico-chemical stresses but also the hydrodynamic conditions pertaining to estuaries. For example, even though the lower estuarine areas have k-strategists such as the tellinid bivalves, the highly variable areas are often dominated by oligochaetes (McLusky et al., 1993) and some zooplankton (e.g. Pseudodiaptomus, Eurytemora and Acartia) have rapid reproduction and development to capitalise on changing estuarine conditions (Jerling and Wooldridge, 1991). There is also a paradox here in that the dominant estuarine organisms are generalists (euryoecious) in terms of broad tolerances but they are also specialists at surviving highly variable conditions. In addition to being generalists in their physiology for salinity tolerance, they also very flexible in terms of dietary adaptations to changing food availability and foraging conditions (Whitfield, 1984).

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Whilst small bodied r-strategists are probably the numerically dominant group in estuaries in both hemispheres, it is possible that larger marine migrant k-strategists may predominate if biomass is used as the measure (Whitfield, 1990). However, this has 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 the opposite view could also be argued. The Estuarine Fish Community Index can sometimes indicate that an estuary is in good condition (i.e. not artificially stressed) although the use of selected biomarkers on individual fish can show that the system is under additional stress (Richardson et al., 2011). Similarly, while stress is often shown at the individual level, it is often more difficult to show this translated to the population or community level (e.g. Borja et al., 2009; García-Alonso et al., 2011). The problem in both hemispheres is that estuarine biotic communities are adapted to high levels of ‘natural’ stress which makes the assessment of ‘artificial’ (anthropogenic) stress difficult (Elliott and Quintino, 2007; Dauvin and Ruellet, 2009). Similarly, it is considered that the natural characteristics of an estuary usually mimic those due to anthropogenic stress, the socalled ‘estuarine quality paradox’ (Elliott and Quintino, 2007). 3. Management-based paradigms

(b) Comments/relevance/support The headwaters and oligohaline regions of many northern hemisphere estuaries are dominated by freshwater species but there is a very poor penetration of freshwater species into the headwaters of most southern hemisphere estuaries, even though this is where the highly productive river-estuary interface region is located (Bate et al., 2002). While the Remane pattern (Remane, 1934) is widely quoted as accounting for this species minimum, there is still a need for evidence that can be applied to all groups of organisms in estuaries, not just the sedentary invertebrate taxa used by Remane (Telesh et al., 2011). Once again, the disjunct at the head (in which river flow ceases for long periods) and mouth (closure occurs for long periods) of many southern hemisphere estuaries disturbs the continuity depicted in the Remane diagram (Remane and Schlieper, 1971). The species richness/abundance/biomass model outlined above applies to estuaries in both hemispheres and is related to ecological tolerances, the presence of opportunists, the abundance of organic material, etc. There is a further paradox that if biodiversity is regarded as relating to a taxonomic basis, then for estuaries this needs to be compared to diversity in physiological response terms. As physiology is a primary driver of the biodiversity that occurs within estuaries, this, in turn, will affect ecosystem functioning in estuaries in both hemispheres. Hence, the Remane diagram is based on the taxonomic diversity of species rather than the diversity of forms using salinity tolerances or physiology as the criteria. As indicated above, those species that can survive estuarine fluctuations qualify for the ‘subsidy’ that these systems provide. However, within any estuarine community (in both hemispheres) there will be those species that qualify for a large subsidy (e.g. estuarine dependent taxa) and those less adapted species that will receive less of a benefit. If one sets aside the physiological specialisations required for a life in estuaries, then generalists (particularly in terms of dietary flexibility, etc) tend to dominate estuaries in both hemispheres, e.g. there are numerous examples of fish species in estuaries switching their diet in major ways according to food availability (Whitfield, 1984). Fish and bird predators especially seem to be generalist and opportunist feeders, hence producing the observed complexity of estuarine foodwebs (e.g. Elliott et al., 2002).

3.1. Pressures, valuing, valuation and management 3.1.1. Paradigm 7 Estuaries have more human-induced pressures than other systems and these include both exogenic unmanaged pressures and endogenic managed pressures. Consequently their management has to not only accommodate the causes and consequences of pressures within the system but, more than other ecosystems, they need to respond to the consequences of external natural and anthropogenic influences. (a) Interpretation/meaning Just as estuaries are dependent on ecological scales and processes from inside and outside the system, so the management of estuaries has to accommodate the consequences of pressures emanating from outside the system (exogenic unmanaged pressures) and the causes and consequences of pressures from within the system (endogenic managed pressures) (Borja et al., 2010; Elliott, 2011). For example, alleviating eutrophication in an estuary requires managing the consequences of nutrients from upstream but within a light regime/ mixing environment created by waves and tides, over which management has no control. Given the pre-eminence of estuaries as favoured sites for urban, port and industrial activities, as well as the anthropogenic pressures emanating from the catchment and marine environment which affect estuarine structure or functioning, then it is likely that estuaries have more pressures than other systems (McLusky and Elliott, 2004). In addition, there are consequences for 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 estuarine 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 we emphasise that anthropogenic influences are superimposed on to natural influences that already place these ecosystems under a large amount of stress. The nested DPSIR approach is perhaps even more relevant to estuaries than for other systems, and in managing estuaries the Ecosystem Approach, which links the natural and socioeconomic 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 (developed from OECD, 1993 and expanded in Atkins et al., 2011); each driver has a DPSIR cycle and there are many such cycles within an estuary (navigation/transport, food provision, infrastructure area, recreation/tourism, etc.), but also there are DPSIR cycles upstream and at sea which affect those in the estuary. For example, demands for food produced by marine fisheries place additional pressures on the estuarine community (which is the nursery area for some of these targeted species) and, unless controlled, will have an impact on catches by depleting estuarine fish stocks. There is also the possibility that reduced marine fish stocks will increase the demand for estuarine sites for aquaculture which will then place increasing pressure on the ecological functioning of the estuary. The Ecosystem Approach sensu stricto relates to management for both ecological and socio-economic benefits (Elliott, 2011). Hence, in the case of applying this to an estuary then the natural and social aspects in the catchment (freshwater and terrestrial areas) and in marine areas (even far from the estuary) have to be considered. Similarly, the management of nature conservation of an estuary has to reflect various scales to cater for the needs of biota from outside the immediate system (Borja et al., 2010). For example, for wading birds and diadromous fishes there are influences associated with the areas they use when not in the estuary; the maintenance of mudflats relies on a sediment supply and tidal regime generated elsewhere, and estuarine plants rely on nutrients supplied mainly from the catchment. Hence the health of an estuary has to be measured not only in terms of internal features but also external influences, e.g. water quality issues associated with some developed (industrialised and urbanised) northern hemisphere estuaries or water quantity problems noted for certain southern hemisphere systems (Whitfield and Elliott, 2002). In both hemispheres, the focus of estuarine health measurements primarily should be on the estuary itself but those outside influences deemed to be impacting on the estuary also have to be considered (e.g. catchment water balance, upstream pollution events). (b) Comments/relevance/support In both hemispheres, the catchment (including the immediate estuary surrounds) should be a focus for any estuary management plan but there are differences in our ability to manage terrestrial, freshwater and some estuarine processes (Lotze et al., 2006; Hering et al., 2010; Borja et al., 2010). There is also the problem in many countries where different government bodies/management authorities are responsible for the management of terrestrial, freshwater, estuarine and marine components (e.g. see Elliott et al., 2006). Getting these different departments/authorities to work together is always difficult and far more complex than, for example, the management of a grassland or forest ecosystem. Exogenic events, especially river flooding (whereby the entire catchment run-off funnels through an estuary) and marine storm-surge events (once again where estuaries are primary recipients of such events), place major pressures on estuaries in both hemispheres. Sea-level rise has to be accommodated by the management (and the ecology) of an estuary (Elliott et al., 2007; FitzGerald et al., 2008) and it has been suggested that these systems are adapted to being ‘reset’ from time to time. Indeed, estuarine ecosystems have to be attuned to being able to respond to radical external influences that transform the habitat at both regular and irregular intervals. Thus the resilience and resistance in estuaries has to be far greater than other aquatic environments that are not subject to these major external pressures.

Even if an estuary is not dominated by them, it is certainly reliant on outside events/processes. The resilient nature of estuaries in both hemispheres means that there is a high degree of internal ‘control’ and flexibility. For example, this is evidenced by the ability of temporarily closed estuaries in South Africa and Australia to function very well in the absence (as long as it is not permanent) of linkages with both the river catchment and marine environment. Unfortunately, the increasing abstraction of freshwater from river systems in the southern hemisphere is placing more extreme pressures on the duration of these linkages, sometimes to the detriment of the estuarine ecosystem (Whitfield and Wooldridge, 1994). Habitat loss is perhaps the major pressure resulting from most estuarine developments in both the northern and southern hemispheres and this places an increasing pressure on the natural functioning of estuaries that are already under considerable natural stress (Chust et al., 2009). Habitat loss may have been temporary, caused by poor water quality from organic and polluting inputs or water removal, or permanent resulting from land-claim and infrastructure building (Elliott et al., 2007). In recent decades, estuarine habitat creation and restoration has been required to deal with the pressures arising from historical habitat loss (Simenstad et al., 2006; Elliott et al., 2007; Lotze, 2010; Zedler and Kercher, 2005). In both hemispheres, any artificial habitat creation is generally at the expense of existing natural habitat or, in many northern areas, in the form of the recovery of previously destroyed habitats (e.g. managed realignment/depolderisation). 3.2. Delivery and protection of ecosystem services 3.2.1. Paradigm 8 Estuaries provide a wider variety of ecosystem services and an increased delivery of societal benefits than many other ecosystems. Hence estuaries are one of the most valuable aquatic ecosystems serving human needs but for this to occur they require functional links with the adjoining terrestrial, freshwater and marine systems. (a) Interpretation/meaning In the case of the functioning of estuaries in relation to the needs of both natural and social systems, there is a requirement to protect and enhance the ecosystem services that relate to natural functioning, while at the same time delivering societal benefits (Atkins et al., 2011; Zedler and Kercher, 2005). It is also widely acknowledged that estuaries are used by society for a wide variety of activities, e.g. transport, harbours, fishing, recreation, human settlements, etc. (O’Higgins et al., 2010). In turn, given the number of natural processes and linkages with upstream catchment and adjacent terrestrial areas, as well as offshore and coastal marine areas, then there may be more ecosystem services and societal benefits provided by estuaries than other aquatic systems (see Atkins et al., 2011 for a table of ecosystem services and societal benefits). Indeed, there has been a change in attitude about freshwater flowing into the sea as being ‘wasted’, to a realisation that the ecosystem services of coastal marine areas are closely tied to estuarine inputs (Lamberth et al., 2009; Stoeckl et al., 2011). (b) Comments/relevance/support The distribution of coastal towns, cities and ports in both the northern and southern hemispheres indicate a distinct preference for estuarine localities due to the ecosystem services and societal benefits that these ecosystems provide (Pinto et al., 2010; Zedler and Kercher, 2005). These settlements exhibit the full range of type, from large international harbours, industrial cities, to retirement villages. The real estate value of land on the

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banks of an estuary in both hemispheres is generally much greater than equivalent land elsewhere in the same region (Beaumais and Laroutis, 2007) and this alone serves to emphasise 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 has not given a too idiosyncratic or personal view. Despite that, the expectation is that other researchers will add to or modify the paradigms outlined above. Paradigms can be a unifying tool in understanding and managing estuaries and we hope that they will provide a focus on the major issues requiring research attention worldwide. Although the paradigms discussed here appear independent of one another and have been given equal weighting, we take the view that some are more crucial to estuarine ecological and management issues than others. We are also aware, as already indicated, of the links between some of the paradigms but feel that the specific issues around each one merit a focused discussion without ‘dilution’ by related paradigms. The listed paradigms also allow us to know the limitations of our science and management, especially if the scientific community is of the opinion that they cannot be tested and defended rigorously. We would especially welcome comments and contributions from the wider estuarine community to modify, expand and perhaps even add to those dealt with in this review. Acknowledgements We gratefully acknowledge the many colleagues and authors who have knowingly or unknowingly contributed to the discussions included in this publication. Similarly we are very grateful to the three anonymous reviewers who provided constructive comments and suggestions on an earlier version of the paper. References Abrantes, K.G., Sheaves, M., 2010. Importance of freshwater flow in terrestrialaquatic energetic connectivity in intermittently connected estuaries of tropical Australia. Marine Biology 157 (9), 2071e2086. Atkins, J.P., Burdon, D., Elliott, M., Gregory, A.J., 2011. Management of the marine environment: integrating ecosystem services and societal benefits with the DPSIR framework in a systems approach. Marine Pollution Bulletin 62 (2), 215e226. Attrill, M.J., 2002. A testable linear model for diversity trends in estuaries. Journal of Animal Ecology 71, 262e269. Attrill, M.J., Rundle, S.D., 2002. Ecotone or ecocline: ecological boundaries in estuaries. Estuarine, Coastal and Shelf Science 55, 929e936. Baird, D., Ulanowicz, R.E., 1993. Comparative study on the trophic structure, cycling and ecosystem properties of four tidal estuaries. Marine Ecology Progress Series 99, 221e237. Baird, D., Winter, P.E.D., Wendt, G., 1987. The flux of particulate matter through a well mixed estuary. Continental Shelf Research 7, 1399e1403. Bate, G.C., Whitfield, A.K., Adams, J.B., Huizinga, P., Wooldridge, T.H., 2002. The importance 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: the case 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 lake system. Biological Journal of the Linnean Society 8, 267e277. Bodineau, L., Thoumelin, G., Béghin, V., Wartel, M., 1998. Tidal time-scale changes in the composition of particulate organic matter within the estuarine turbidity maximum zone in the macrotidal Seine Estuary, France: use of fatty analysis and sterol biomarkers. Estuarine, Coastal and Shelf Science 47 (1), 37e49. Borja, Á, Elliott, M., Carstensen, J., Heiskanen, A.S., van de Bund, W., 2010. Marine management e towards an integrated implementation of the European marine Strategy framework and the water framework directives. Marine Pollution Bulletin 60, 2175e2186. Borja, Á, Muxika, I., Rodríguez, J.G., 2009. Paradigmatic responses of marine benthic communities to different anthropogenic pressures, using M-AMBI, within the European Water Framework Directive. Marine Ecology 30, 214e227. Boyes, S.J., Elliott, M., 2006. Organic matter and nutrient inputs to the Humber Estuary, England. Marine Pollution Bulletin 53 (1e4), 136e143.

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