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The overall aim of the approach described here is to help understand, explain and eventually use in a management context, the functioning of estuaries and especially the use of these areas, many of which have been perturbed by human activities (Jackson et al. 2001, Warwick et al. 2018). Hence, it is particularly important to determine the food webs, predator‐prey relationships and carrying capacity of estuaries, and the effects on these as a result of anthropogenic, hydromorphological and chemical modifications. This requires an understanding of the feeding mode of fish species when they are within the estuary, irrespective of foraging mode while they are in any adjacent habitat. For example, Hostens and Mees (1999) analysed feeding guilds in an estuarine environment and found that, while certain fish species depended on the hyperbenthos (i.e. the mobile forms on or just above substratum) in the estuary, they take other prey when outside the estuary. Also, a comparison of large fish predator diets in an estuary found that dietary diversity was greater there than on the adjacent inner continental shelf (Able et al. 2017). Therefore, in the approach used here the Feeding Mode Functional Group (FMFG) relates to the diet of a species while in the estuary, acknowledging that, given the often opportunistic nature of feeding by most fishes associated with these systems (e.g. Nemerson & Able 2004), some taxa will be difficult to assign to a particular group. When it is not possible to assign a species because of a very wide set of feeding preferences, that species should be regarded as miscellaneous/opportunistic, hence the inclusion of this category in Table 2.3.

Essentially, the FMFG classification of Elliott et al. (2007) is a trophic guild system designed to allow fish species that utilise similar food resources to be aggregated. The classification draws upon other fish feeding guilds such as that developed by Elliott & Dewailly (1995) for European fishes, as well as a standardised table of fish food items provided in FishBase (Froese & Pauly 2006) and identifies seven broad categories, viz. detritivore, herbivore, omnivore, zooplanktivore, zoobenthivore, piscivore and miscellaneous/opportunist (Table 2.3, Figure 2.11).

The detritivore category includes those species that feed on decaying organic (plant or animal) matter along with the associated bacteria and fungi, sometimes referred to as benthic floc. Although most detritivores also consume benthic microalgae (microphytobenthos) (Whitfield & Blaber 1978), it is often unclear whether the detritus/benthic floc or microphytobenthos is the targeted food source. Mugilids, for example, feed on organic matter and diatoms off the substratum and have a muscular gizzard‐like stomach designed for physical grinding (using ingested sediment) of this algal and detrital material (Cardona 2016). Similarly, the term iliophagous (sediment‐feeding, sensu Bowen 1979) can be used as an indication that fish are ingesting the sediment, together with its detritus, microphytobenthos and small associated fauna, e.g. meiofauna. In view of this, and to prevent the creation of a large number of terms, the detritivore category has been extended from previous analyses (e.g. Elliott & Dewailly 1995, Potter & Hyndes 1999) to include those fish that consume microphytobenthos, detritus, sediment and small associated fauna.

The herbivore category includes fishes that consume plant material and although few, if any, estuarine‐associated species are reported to ingest only phytoplankton, the subcategory herbivore‐phytoplankton is included to accommodate phytoplanktivorous fishes should new information on fish diets become available. Hajisamae et al. (2003), for example, reported that phytoplankton dominated the diet of the clupeid Anodontostoma chacunda in the Johor Strait estuarine system in Singapore. FishBase also includes phytoplankton as a subset of the plant food category (Froese & Pauly 2006) and, in the assessment by Elliott et al. (2007), the herbivore category accommodates those fishes that have a mainly herbivorous diet comprising large plants or phytoplankton (Table 2.3).

Table 2.3 Feeding Mode Functional Group (FMFG) (modified from Elliott et al. 2007).

Category	Definition	Examples
Cool/warm temperate	Subtropical/tropical
Herbivore (HV)	Grazing predominantly on living macroalgal and macrophyte material or phytoplankton.	Sarpa salpa (Sparidae)	Coptodon rendalli (Cichlidae)
Omnivore (OV)	Feeding predominantly on filamentous algae, macrophytes, periphyton, epifauna and infauna.	Diplodus sargus (Sparidae) Rhabdosargus holubi (Sparidae) Hyporhamphus capensis (Hemiramphidae)	Chanos chanos (Chanidae) Arrhamphus sclerolepis (Hemiramphidae) Siganus vermiculatus (Siganidae)
Detritivore (DV)	Feeding predominantly on benthic detritus, microphytobenthos and associated meiofauna.	Mugil curema (Mugilidae) Chelon richardsonii (Mugilidae)	Mugil cephalus (Mugilidae) Oreochromis mossambicus (Cichlidae)
Zooplanktivore (ZP)	Feeding predominantly on zooplankton (e.g. planktonic crustaceans, fish eggs/larvae).	Sprattus sprattus (Clupeidae) Engraulis australis (Engraulidae) Gilchristella aestuaria (Clupeidae)	Tenualosa toli (Clupeidae) Thryssa vitrirostris (Engraulidae) Hilsa kelee (Clupeidae)
Zoobenthivore (ZB)	Feeding predominantly on invertebrates associated with the substratum, including zoobenthos and hyperbenthos.	Pleuronectes platessa (Pleuronectidae) Cnidoglanis macrocephalus (Plotosidae) Sillaginodes punctatus (Sillaginidae)	Acanthopagrus australis (Sparidae) Pomadasys commersonnii (Haemulidae) Pomadasys kaakan (Haemulidae) Sciaenops ocellatus (Sciaenidae) Anchoa mitchilli (Engraulidae)
Opportunist (OP)	Feeding on a diverse range of food and cannot be readily assigned to one FMFG.	Platichthys flesus (Pleuronectidae) Amniataba caudavittata (Terapontidae)	Bairdiella chrysoura (Sciaenidae) Terapon jarbua (Terapontidae)
Piscivore (PV)	Feeding predominantly on finfish but may include large nektonic invertebrates.	Argyrosomus japonicus (Sciaenidae) Lichia amia (Carangidae) Pomatomus saltatrix (Pomatomidae)	Sphyraena jello (Sphyraenidae) Caranx sexfasciatus (Carangidae) Scomberoides commersoniannus (Scombridae)

Figure 2.11 Examples of fish species from each Feeding Mode Functional Group (FMFG, see Table 2.4 for more details) from southern African estuaries (after Whitfield 2019).

There appear to be very few examples of exclusive herbivory among the fishes found in estuaries, possibly due to their lack of a cellulase with which to digest the cell walls of plants (Kapoor et al. 1975). Hence, the designation of the herbivorous FMFG may be difficult, especially as most herbivorous fishes in estuaries also consume animal material and often small invertebrates associated with macrophytic plants and filamentous algae. Indeed, in most cases it would be almost impossible for a fish foraging on plant material not to also ingest small invertebrates associated with the vegetation. In some cases, the fish may be targeting the periphyton and epifauna associated with the plants, rather than the leaf blades on which these biota exist. An example of such a fish in estuaries is Diplodus capensis from southern Africa, which consumes wide spectrum of biota, especially aquatic macrophytes, filamentous algae and the associated epifaunal and periphyton (Coetzee 1986). Another species, Pelates octolineatus, consumes predominantly small crustaceans when <50 mm total length, but has an almost exclusively herbivorous diet at larger body sizes (Poh et al. 2018).

In some cases, there may be a temporal separation of food, e.g. Hyporhamphus capensis consumes mainly zooplankton in late winter and macrophytic plants in late summer (Coetzee 1981). At a finer scale, the congeneric Hyporhamphus melanochir consumes seagrass during the day, but benthic‐dwelling amphipods at night following their nocturnal vertical migration (Robertson & Klumpp 1983). There is the need for an energetic assessment of this type of feeding in that, although a large amount of plant material is ingested by these species, the relatively small amount of animal material may be more important to the fish because of the higher calorific value and assimilation rate. For example, although H. melanochir consumed three times more seagrass than crustaceans, these invertebrates were considered by Klumpp & Nichols (1983) to be an essential source of protein and be at least as important as seagrass in providing energy. While there may not be many true herbivores in estuaries, there are some, such as certain Hemiramphidae, Sparidae, Siganidae and Kyphosidae, in which their diet is overwhelmingly dominated by plant material (Nordlie & Kelso 1975). It is therefore proposed that the herbivore category be retained for further testing, especially as a means of comparing fishes in different systems.

Zooplanktivorous fishes are those that typically feed on small crustaceans in the water column, for example the diet of Anchoa mitchilli comprises mainly zooplankton but may also include fish eggs and larvae (Froese & Pauly 2006). Typical zooplanktivores found in estuaries include members of the Clupeidae and Engraulidae (Table 2.3). Zooplankton is also a major component of the diet of the larvae of marine fish species (Llopiz 2013) and most, if not all estuary‐associated fish species, are planktivorous during their larval life (Islam et al. 2006), but change to juvenile/adult diets with growth (Whitfield 1985, Strydom et al. 2014). The larvae of many anadromous, semi‐anadromous and estuarine‐resident fishes also prey predominantly on zooplankton (Costalago et al. 2016) and are therefore part of the zooplanktivorous guild at this stage of their life cycle. The majority of marine fishes that utilise estuaries, however, enter these systems as postlarvae and are therefore already at a stage where they have or are about to switch to their juvenile/adult diet (Strydom et al. 2014). In addition, there are examples of pelagic fish taxa such as Hilsa, Alosa and Brevoortia, which consume zooplankton during both the larval and juvenile stages (Blaber 1979). Juveniles and adults of several species of atherinid in south‐western Australia have been shown to consume large quantities of planktonic crustaceans (Prince et al. 1982).

Many bottom‐dwelling fishes feed on organisms associated with the substratum (zoobenthos), hence the terms zoobenthivore and benthophagous. Zoobenthos includes animals that live in the sediment (infauna), on the sediment (epifauna), or immediately above the sediment (hyperbenthos) and the term benthophagous can also include flora associated with the benthos. The term hyperbenthophagous fish species has also been identified, i.e. they are adapted to feeding on the hyperbenthos, i.e. those mobile organisms living just above the substratum (Sibert 1981). Thus, while hyperbenthophagous species could be regarded as a subgroup of the zoobenthos feeders, their prey sources will require different methods of capture and have thus been kept separate by Elliott et al. (2007). In general, many benthic/demersal fish species feed on fauna that are associated with the sediment. Since much of the zoobenthos (especially the epifauna) is sometimes in, sometimes on and sometimes above the sediment (e.g. many amphipods) according to the time of day, tidal regime, current flow rates, etc. (Read & Whitfield 1989, Rose et al. 2020), it is often difficult in practice to separate these two compartments. Furthermore, for most species, detailed feeding behaviour is unknown and likely to remain so in turbid estuaries.

While it is difficult to separate the zoobenthic components, the three subdivisions: zoobenthivore‐hyperbenthos, zoobenthivore‐epifauna, and zoobenthivore‐infauna created by Elliott et al. (2007) do accommodate any new information on fish diets that become available. For example, in recent decades, hyperbenthophagous fish species have been identified since their diet and method of feeding are centred on those mobile organisms living just above the estuary bottom. In addition, certain fish species have developed specialised feeding mechanisms to exploit infauna. For example, Pomadasys commersonnii and Lithognathus lithognathus both have protrusible mouthparts and employ a gill chamber pump action to extract mud prawns from their burrows (van der Elst 1988). Some fish species also deliberately target certain infauna or parts of their prey, e.g. members of the Gerridae in the Kosi Estuary, South Africa (Cyrus & Blaber 1982) and Soleidae in the Humber Estuary, UK (Marshall 1995) feed by cropping bivalve siphons. The possible impact of siphon nipping by fishes on bivalves has been investigated by Coen & Heck (1991) and shown to significantly reduce growth of the mollusc.

The piscivore category includes large carnivorous species that feed mainly on other fishes. Although estuaries provide shelter from major fish predators, several estuary‐associated fishes are piscivorous. Examples include members of the Carangidae, Elopidae, Gadidae, Pomatomidae and Sciaenidae (Table 2.3). While piscivores feed primarily on fishes, they will also consume other prey items. In the estuarine Lake St Lucia, for example, swimming prawns (Penaeidae) form a substantial component of the diet of both Argyrosomus japonicus and Elops machnata at certain times (Whitfield & Blaber 1978). There is also a trend for piscivory within this category to increase with increasing body size (Juanes et al. 2001, Nemerson & Able 2003). In recent years the role of small piscivorous predators has become more obvious, including in Australia (Baker & Sheaves 2005) and North America (Able et al. 2007, Musumeci et al. 2014).

In addition to finfish, FishBase includes cephalopods (squid and cuttlefish) within the nekton food category (Froese & Pauly 2006). FishBase also contains a category ‘other’ which includes food items such as reptiles, birds and mammals that are typically consumed by apex predators such as sharks. Apex fish predators are generally absent from estuaries although Carcharhinus leucas enters large estuarine bays, lakes and rivers. In South Africa, however, the individuals found in estuaries are usually juveniles whose diet is dominated by fishes (D'Aubrey 1971).

Those species that fit into the ‘other’ category should be relatively consistent in their prey/food choice in a range of estuaries, but this is not always the case (Able et al. 2017). Given the nature of feeding by many estuary‐associated species, however, there is a need for an opportunist category, which is separate from the omnivore category and used for those species that are opportunist but not necessarily omnivorous. Examples of estuarine omnivores include Diplodus capensis from southern Africa (Coetzee 1986), Acanthopagrus butcheri in south‐western Australian estuaries (Sarre et al. 2000, Chuwen et al. 2007) and Lagodon rhomboides from North American east coast estuaries (Stoner 1980, Darcy 1985). Both species ingest a wide spectrum of animal and plant food items, especially aquatic macrophytes, filamentous algae and the associated epifauna and periphyton. Although these species are opportunistic in that the proportions of major dietary categories consumed varies greatly among estuaries, this opportunism should not influence the primary FMFG categorization which is driven at a higher level of resolution.

An opportunist species is likely to feed on very different prey/food in different estuaries depending on food availability, whereas omnivores will probably have a dietary mix of plant and animal material in different areas. The term opportunistic has been used by Elliott et al. (2007) to indicate both the feeding behaviour and food preferences of fish, rather than food preferences alone. It is increasingly observed that many estuarine fishes take almost any suitably sized prey that they encounter and should thus be regarded as opportunists. For example, the flounder P. flesus may take infaunal benthos, epifaunal shrimps or zooplankton, depending on prey availability and size of the individual fish (Costa & Elliott 1991).

Thus, while the EUFG reflects the migratory behaviour and physiological tolerances of fishes, the FMFG reflects the feeding behaviour and their body structure as an adaptation to feeding on particular prey, i.e. their ecotrophomorphology or ecomorphology (Wootton 1990). For example, streamlined clupeids inhabiting the water column have relatively large terminal mouths and feed on zooplankton and therefore have a very different ecomorphology to that of demersal sparids, which have subterminal mouths and prey on hyperbenthic crustaceans using protrusion, suction and pivot foraging methods.

The southern African sparid R. holubi is an omnivore that always ingests both plants and animals where both of those food sources are available (Blaber 1974). Where aquatic macrophytes are unavailable, it will actively search for alternative plant material, and then, for example, feed on filamentous algae growing on the stems of Phragmites reeds as in the Mhlanga Estuary (Whitfield 1980b). In the Swartvlei system, the diet of R. holubi was dominated by both pondweed Stuckenia and associated epifauna, but when the macrophytes disappeared from the littoral zone it consumed the filamentous algal mats that replaced the Stuckenia and the epifauna associated with the sediments (Whitfield 1984). When the algal mats also disappeared, this sparid became restricted to a carnivorous diet (epifauna associated with the sediments) and its body condition, as reflected in the length/weight relationship, declined. Thus, while juvenile R. holubi may survive on a carnivorous diet, they require an omnivorous diet to thrive and select both plant and animal material when available.

The FMFG classification of Elliott et al. (2007) provides a method of grouping fishes according to common broad dietary categories. However, it is becoming increasingly evident that many estuarine‐associated fishes are opportunistic in that they switch their diet beyond their ‘normal’ spectrum, as and when opportunities arise. Such opportunistic feeding behaviour sometimes makes it difficult to assign a species to a particular feeding category. While most estuarine‐associated fishes are to a certain extent opportunistic, Elliott et al. (2007) proposed that a FMFG classification should be based on the normal or preferred diet of a species. An opportunistic category was created by the above authors, however, to accommodate situations where a species cannot be placed in one of the more conventional FMFG categories. This opportunistic category should not be confused with the omnivore category, which includes those species with a regular, varied diet of both plant and animal material.

The diets of most estuary‐associated fish species also undergo ontogenetic shifts. During their larval life most fishes are planktivorous but switch to juvenile diets at lengths that vary according to the taxa (Blaber & Whitfield 1977, Strydom et al. 2014). Some species such as Mugil cephalus retain the same feeding mode through the juvenile and/or adult life stages (Blaber 1976). The types of food consumed by certain other species, however, change markedly with growth. For example, Gadus morhua is a planktonic feeder as a larva, benthophagous as a 0+ juvenile, then consumes hyperbenthic crustaceans such as mysids and pericarid shrimp, before becoming a piscivore when mature (Costa & Elliott 1991). Thus, this group of species will move from one feeding category to another during their lives. Where possible, ontogenetic changes in diet should be accounted for by allocating the diets of the various size classes to the appropriate FMFG category. In practice, however, this may be difficult and an alternative may be to allocate a FMFG category to a particular species based on the diet of the predominant size classes or life cycle stage (e.g. mostly juveniles) present within an estuary.

While it is recognised that estuaries form an important function for a number of fish species, many of the species found in estuaries are marine stragglers and not dependent on these environments. Furthermore, many diadromous species such as all lampreys and certain salmonids and anguillid eels do not feed while passing through the estuary, especially the mature individuals on their final spawning migrations (Froese & Pauly 2006). It is recommended by Elliott et al. (2007) that a feeding guild analysis should be restricted to the dominant Estuarine Use Functional Groups (EUFG) occupying a particular system, i.e. those fish species that are common and forage mainly within the estuary. For example, marine stragglers, catadromous and anadromous groups should not be included in a FMFG analysis.