The trophic level of fish forms an important part of understanding the structure and dynamics of food webs in aquatic ecosystems. Trophic level estimates have typically relied on either diet and feeding studies, or stable isotope analyses. This study used trophic level values provided in FishBase (Froese & Pauly, 2023), which is based on food and diet data. A close correlation has been reported for trophic level estimates in marine ecosystems based on food items and stable isotope ratios in the cold-temperate Prince Willian Sound (Kline & Pauly, 1998) and Barents Sea (Pedersen, 2022), the warm-temperate Bay of Biscay (Lassalle et al., 2014), Adriatic Sea (Mancinelli et al., 2013), East China Sea (Gao et al., 2021), and Laguna de Rocha, Uruguay (Milessi et al., 2010), and tropical Indonesia (Du et al., 2020).
This study also found a good relationship between trophic level values and fish feeding mode functional groups. A similar strong association between fish functional feeding groups and their trophic levels was reported by Whitfield et al. (2022) for some 255 fish species occurring in European estuaries; detritivorous and herbivorous fishes had mean trophic levels of 2.7 and 2.9 respectively; zooplanktivores and zoobenthivores were between 3.4 and 3.5, while piscivores had a mean trophic level of 4.0. An analysis of the feeding habits and trophic levels of Mediterranean fish (Stergiou & Karpouzi, 2002) identified several trophic functional groups; herbivores had a mean trophic level of 2.0, omnivores with a preference for vegetable material had a mean trophic level of 2.5, and omnivores with a preference for animal material had a mean trophic level of 3.4. Two groups of carnivores were identified, one exhibiting a preference for decapods and fish (mean trophic level = 3.9) and the other exhibiting a preference for fish and cephalopods (mean trophic level = 4.4) (Stergiou & Karpouzi, 2002). A cluster analysis based on a stable isotope study of the food web of the tropical Sine Saloum Estuary, Senegal, identified several trophic groups of fishes (Faye et al., 2011). Fishes that fed on organic matter and benthic microalgae had a mean trophic level of 2.8, while species that were predominantly pelagic feeders had a mean trophic level of 3.1; fishes that were predominantly benthic invertebrate feeders had a mean trophic level of 3.6, and piscivores had a mean trophic level of 4.4 (Faye et al., 2011).
This study has shown that significant differences exist between bioregions both in terms of their trophic levels and feeding functional guilds. A cluster analysis of functional guilds, including feeding guilds, in European estuaries identified several geographical groupings that included Mediterranean estuaries, Baltic estuaries, and North Sea and Atlantic systems (Franco et al., 2008). A comparative zoogeographic analysis of the fish trophic structure of South African estuaries (Harrison & Whitfield, 2012) also reported biomass differences in the trophic spectrum profiles and feeding guild composition of different estuary types within the various biogeographic regions identified.
Overall, zoobenthivores dominated the relative fish species composition in all bioregions during this study. In a global analysis of estuarine fish functional traits, Henriques et al. (2017) also found that invertivore fishes dominated estuarine fish assemblages both in terms of relative species composition (47%) and relative abundance (40%). Benthic invertebrate feeding fishes were also found to dominate the fish communities in temperate European estuaries (Elliott & Dewailly, 1995; Mathieson et al., 2000; Franco et al., 2008). This group were also among the dominant group in tropical estuaries in the Indo-Pacific (Sreekanth et al., 2000; Kumar et al., 2023) and tropical West Africa (Faye, 2011). Zoobenthivores were the dominant feeding guild of fishes in the warm-temperate Patos Lagoon Estuary, Brazil (Mai & Possamai, 2022). Using data compiled from several studies, Whitfield (2019) also noted that zoobenthivores dominated the relative fish species composition of both subtropical and warm-temperate South African estuaries and comprised between 32 and 48% of the taxa. Data from Sheaves et al. (2016) revealed that zoobenthivores (macrobenthivores and microbenthivores) dominated the taxa reported in tropical estuaries in north-eastern Australia.
The main food of most benthic invertebrates comprises a mixture of detritus, phytoplankton and benthic microalgae (Whitfield, 1989; Svensson et al., 2007). The detritus is derived primarily from aquatic macrophytes, phytoplankton, microphytobenthos and epiphytic algae, with both authochthonous and allochthonous sources playing a role (Haines & Montague, 1979; Schlacher and Wooldridge, 1996; Connolly et al., 2005). Zoobenthos and micro-organisms greatly assist in the breakdown of macrophytic leaves into detritus (Schleyer, 1986; Haram et al., 2020), thus making this material available as a food source to a variety of zoobenthivorous fish species via invertebrate prey (Whitfield et al., 2024). It is important to note that detritus confers stability to the trophic functioning of estuarine ecosystems since it is available in large quantities throughout the year, regardless of latitude. This study has shown that detritus is cycled through estuarine fish assemblages in tropical and subtropical estuaries directly by detritivorous fish species and indirectly through zoobenthivorous fish species utilizing the invertebrate food chain, but primarily indirectly through benthic invertebrates and zoobenthivorous fish species in cool temperate estuaries.
The trophic spectrum analysis showed that, although statistically significant differences were observed between arid, tropical and warm-temperate bioregions, this was relatively weak; all these bioregions had somewhat similar profiles. The profile of tropical ecoregions, however, was generally above other ecoregions, which suggests a higher contribution of fish taxa that feed at relatively lower trophic levels. This is also reflected in the relatively lower mean trophic level recorded in this bioregion and the relatively higher contribution of detritivores, herbivores and omnivores. These feeding guilds showed a general decline from tropical ecoregions to warm-temperate and cool-temperate ecoregions with the relative species contribution of these groups of fishes being significantly lower in cool-temperate ecoregions than that recorded in tropical ecoregions. The relative proportion of detritivores, herbivores, and omnivores also showed a positive correlation with temperature.
The higher fish species diversity and richness in tropical versus temperate estuaries parallels global temperature trends (Harrison & Whitfield, 2022; 2024) and may be directly or indirectly responsible for the wider array of fishes in different trophic categories, as well as the higher diversity of food resources in tropical versus temperate estuaries. Henriques et al. (2017) also reported a positive correlation in the proportions of detritivore, herbivore, and omnivore fishes in estuaries globally that was strongly associated with increasing sea surface temperature. They suggested that this may be related to the higher efficiency in digestion of plants and detritus in warmer waters than in cooler conditions; it would be more difficult for these feeding guilds to meet their metabolic demands at cooler temperatures (Henriques et al., 2017). Franco et al. (2008) noted that detritivory was scarce in fishes from European estuaries and was largely confined to warmer Mediterranean systems. Furthermore, despite the relatively high standing stocks of macroalgae, herbivory was also an infrequent and highly variable feeding mode in European temperate estuaries. They also report a decline in herbivorous fishes with latitude and suggest that lower temperatures limit food-processing rates with a need for more energy-rich (animal) food sources (Franco et al., 2008).
A decline in the relative abundance of herbivorous fishes (including detritivores) with increasing latitude has also been reported in western Atlantic and Brazilian reef fishes (Floeter et al., 2004; Ferreira et al., 2004). A global analysis also reported a highly significant negative relationship between latitude (and positive between mean sea surface temperature) and both the relative abundance and relative richness of herbivorous (and detritivorous) fishes worldwide (Floeter et al., 2005); this was most marked at temperature ranges below 20°C. It was suggested that the distribution of herbivorous fishes was not a result of the availability of algae present but rather due to temperature-related feeding and digestive processes of fishes in these systems (Ferreira et al., 2004; Floeter et al., 2004; 2005); some herbivores and omnivores appear to overcome this temperature constraint through increasing animal protein in their diet.
This study found a significant positive association between estuarine macrophyte vegetation and the relative contribution of herbivores and omnivores and, although the relative proportion of detritivore, herbivore, and omnivore fish species declined from tropical to warm- and cool-temperate bioregions, the trophic level of these feeding guilds increased from tropical to warm-temperate and cool-temperate bioregions. This study also reported a significant negative relationship between the trophic level of detritivores and omnivores with sea surface temperature; this suggests that these groups of fishes consume higher trophic level food at higher latitudes. Floeter et al. (2004) noted that in colder peripheral sites, such as the Mediterranean, fishes that feed on intermediate-quality food (omnivores) have higher abundance and diversity, compared to warmer sites and that these fishes could exploit low-nutritional plant and detrital resources only if they are augmented with substantial proportions of high energy animal protein.
The higher representation of detritivorous fish species in tropical and subtropical estuaries can also be attributed to the species richness of Mugilidae in these systems. Whitfield & Durand (2023) have shown that this diverse detritivorous fish family has the greatest species richness in tropical regions and these taxa do not extend into high latitude estuaries in either the northern or southern hemispheres. Although a high proportion of the diet of mugilids consists of detrital material, especially particulate organic matter (Blaber, 1976), this family also depends on microphytobenthos as a food source which is likely to be more productive on intertidal flats of low rather than high latitude estuaries (where photosynthetic conditions are more limited). The detritivorous Cichlidae that occupy estuaries (Whitfield & Blaber, 1978a) also have the highest species richness and abundance in tropical and subtropical systems (Blaber, 2000), thus boosting this feeding guild in warmer parts of the world.
Detritivores, herbivores, and omnivores were well represented in arid ecoregions in this study. Sea surface temperatures of arid ecoregions generally exceeded 20°C with sea surface salinities mostly above 35 psu; they also support a relatively diverse and abundant aquatic and emergent macrophyte vegetation (Harrison & Whitfield, 2024). Abundant food resources and relatively high temperatures probably allow these feeding guilds to utilise estuarine environments in arid ecoregions. In a study of the fish community structure of the coastal fishes of the arid Dampier region of north-western Australia, Blaber et al. (1985) found that Iliophagous (detritivorous) species were abundant in the mangrove creeks where the organic content of the sediment was comparable with other areas of the tropical Indo-Pacific, despite the lack of freshwater inflow. Harrison & Whitfield (2012) also found that detritivorous fishes dominated the biomass composition of estuaries on the arid west coast of South Africa. Detritivores were also positively correlated with salinity during this study. Henriques et al. (2017) found that hypersaline estuaries tended to have more brackish (euryhaline) fishes which were more frequently detritivores, herbivores, and omnivores and that these fishes were probably taking advantage of the lower inter-specific competition and predation offered by these estuaries.
Zooplanktivores exhibited an increase from tropical ecoregions to warm-temperate and cool-temperate ecoregions in this study; this group also displayed a negative correlation with temperature which is likely to be related to latitude. In their global analysis of estuarine fish functional traits, Henriques et al. (2017) also reported a strong association of planktivores in estuaries with cooler waters. An analysis of fish functional guilds in European estuaries (Franco et al., 2008) observed that plankton feeders were particularly abundant in estuaries from the Baltic and North Seas.
In a study of the nearshore fish communities of Portugal, Baptista et al. (2019) found that both the abundance and biomass of planktivorous fish species decreased with a decrease in latitude. A global study of oceanic zooplankton composition and size structure (Brandao et al., 2021) reported an increase in the abundance and size of zooplankton communities towards the poles and that temperature and oxygen were key parameters in driving this pattern. Larger zooplankton enhance energy transfer to higher trophic levels (Brandao et al., 2021) and together with the high abundance of zooplankton at higher latitudes, probably contributes toward the increased relative contribution of zooplanktivorous fishes in cool-temperate ecoregions relative to warm-temperate and tropical bioregions. This study also found that the trophic level of zooplanktivourous fishes was significantly higher in cool-temperate ecoregions than in warm-temperate and tropical bioregions; the trophic level of zooplanktivores was also negatively correlated with sea surface temperature. This suggests that zooplanktivores at lower latitudes consume lower trophic level food than those at higher cool-temperate latitudes. The negative association in terms of both the relative species contribution and trophic level of zooplanktivore fishes with aquatic macrophyte vegetation during this study is probably a reflection of the pelagic lifestyle of this group of fishes. Aquatic macrophytes are typically characteristic of shallow, littoral habitats (Whitfield, 2017).
Piscivores during this study exhibited a general decline from tropical ecoregions to cool-temperate ecoregions, again reflecting the decline in species richness of this guild from the tropics to polar regions. The relative contribution of this group also showed a significant positive correlation with sea surface temperature. Henriques et al. (2017) found that fishes with macrocarnivore diets tended to increase in importance in estuaries of cooler regions; this feeding group, however, included fishes with a diet that included both macroinvertebrates and vertebrates (mostly fishes). In their study of the nearshore fish communities along the Portuguese coast, Baptista et al. (2019) reported an increase in the abundance and biomass of piscivores with a decrease in latitude. Ferreira et al. (2004) found that carnivorous and piscivorous fishes were proportionally more abundant at higher latitudes in Brazilian tropical and subtropical reefs; however, part of this pattern was attributed overfishing of these top predators in the lower latitude Brazilian coastal regions. They also concluded that large carnivores, including piscivores, are not constrained by the thermal thresholds that limit herbivorous fishes and extend farther into high-latitude habitats (Ferreira et al. 2004).
The highest contribution of piscivores was reported in arid ecoregions during this study. This may be linked to the relatively high proportion of detritivore prey species that characterise these ecoregions although the trophic level of piscivores in arid ecoregions suggests the consumption of higher trophic level prey in relatively clear water that favours foraging by visual predators. Blaber et al. (1985) found that piscivores were among the dominant fishes of mangrove creeks of the arid Dampier region of north-west Australia based on relative species composition, numerical abundance, and relative biomass contribution; with the clear and deep water, particularly at high tide, favouring the predation on juvenile fishes by this group. This study found that the trophic level of piscivorous fishes was significantly higher in cool-temperate ecoregions than other bioregions. This may be linked to the relatively higher abundance of low trophic level fish prey species such as herbivores and detritivores in warmer, low latitude ecoregions.
Detritivorous and herbivorous fishes bypass steps in the food web and telescope primary production to fish yield (Cardona, 2016); this effectively lowers the trophic level of piscivorous fishes that prey on these species in tropical and subtropical waters. Based on the results of trophic modelling, Ray & Straskraba (2001) found that detritivorous fishes played a significant role in overall estuarine fish production, particularly as a food source for carnivorous fishes at low latitudes. Piscivorous fishes have also been reported feeding opportunistically on lower trophic level macroinvertebrates such as penaeid prawns in proportion to their seasonal density in tropical estuaries in South Africa (Whitfield & Blaber, 1978b), Australia (Salini et al., 1990), United States (Blewett et al., 2006), and Brazil (Ferreira et al., 2019).
While the relative species contribution and trophic level of the fish feeding functional groups included in this study exhibited significant relationships with several environmental parameters, temperature appeared to be the factor common to most guilds. This was also supported by the overall multivariate analyses based on trophic spectra and feeding mode functional groups. The higher temperatures associated with low latitude tropical ecoregions allow fishes to utilise low quality (trophic level) food while the lower temperatures associated with high latitude cool-temperate regions require energy rich (higher trophic level) food to meet their energy requirements. This pattern is also exhibited in the increase in the overall trophic level of fishes from tropical ecoregions to warm-temperate and cool-temperate ecoregions.
In a global analysis of body size and trophic level of marine fishes Lin & Costello, (2023) found that mean body size and mean trophic levels of marine fish were lower in the tropics and sub-tropics than at high latitudes and that the primary factor associated with this pattern was temperature. They suggested that the warm temperature in the tropics results in shorter generation times, higher rates of metabolism, faster maturation, and faster selection pressure, which generate and maintain high species and functional diversity; the high habitat complexity of tropical and subtropical regions also allow species diversity and trait diversity to originate and accumulate in the tropics and subtropics (Lin & Costello, 2023).
A final issue that requires comment is trophic redundancy in global estuaries. Previous information in this discussion has indicated that there is a decline in detritivorous and herbivorous fish species in estuaries from the topics to high latitudes. This review has therefore highlighted the potential decrease in redundancy from tropical to cool-temperate estuaries, a topic that was highlighted by Whitfield & Harrison (2021). In the context of global estuaries, the level of redundancy for detritivorous, herbivorous and even omnivorous fish feeding guilds declines from the tropics towards the temperate regions as the numbers of fish species belonging to these particular guilds declines with increasing latitude.