- Open Access
Differences in trophic resources and niches of two juvenile predatory species in three Pangani estuarine zones, Tanzania: stomach contents and stable isotope approaches
© The Author(s) 2018
- Received: 2 November 2017
- Accepted: 22 June 2018
- Published: 3 July 2018
Estuaries are primary habitats that serve as feeding and nursery grounds for most juvenile marine fish. However, estuaries have been used as fishing grounds by the artisanal fishers in Tanzania. The slow-growing predatory fish at juvenile and sub-adult stages are among the most frequently caught species that functionally enhance multiple linkages of energy pathways within the food web. Stomach contents and stable isotopes (δ13C and δ15N) were used to describe the nutritional sources and trophic niches between the co-existing benthic, predatory species, Carangoides chrysophrys and Epinephelus malabaricus in the Pangani estuary, Tanzania.
The findings indicated significant inter-specific variations in dietary composition (PERMANOVA, p = 0.001, pseudo-F = 15.81). The prey-specific index of relative importance (%PSIRI) indicated that juvenile shrimps (%PSIRI = 51.4) and Teleostei (%PSIRI = 26.5) were the main diets of C. chrysophrys while brachyura (%PSIRI = 38.8), juvenile shrimps (%PSIRI = 25.6) and Teleostei (%PSIRI = 23.3) were important diets of E. malabaricus. The isotope mixing models indicated that the predatory fish species accumulate nutrients derived from similar autotrophic sources, microphytobenthos, seagrass and macro-algae via consumption of small fish, including clupeids and mugilids. Yet, they significantly showed different isotopic niche width with varying degree of niche overlap across the longitudinal estuary gradient. This situation was justified by the presence of basal food sources among the estuarine zones that isotopically were different.
The reliance of both predators on clupeids and mugilid preys that are trophically linked with estuarine and marine basal food sources, is an indication of low estuarine food webs’ connectivity to the fresh water related food web. This situation is most likely threatening the stability of the estuarine food web structure. Management strategies and plans in place should be cautiously implemented to ensure the balanced anthropogenic freshwater use in the catchment and fishing activities, for the maintenance of the Pangani estuarine ecosystem health.
- Juvenile fish
- Trophic resources
- Pangani estuary
The stability of the food web structure is one of the main determinants of an ecosystem’s health . Preservation of estuarine food web structure is thus vital for maintaining the ecological and functional roles of an estuarine ecosystem. Estuaries in the world are primary habitats for the growth and survival of most juvenile marine fish [2, 3]. They serve as nursery grounds since they provide diverse food and shelter for most marine fish across all trophic levels along the estuarine food web [4, 5]. Such fish community assemblages comprise predatory fish which are economically and ecologically important in the mangrove estuaries along the coast of Tanzania. In these habitats, artisanal fishers tend to fish unselectively by using inappropriate fishing gears . This is a concern especially when the species caught include slow-growing fish that attain large body size before reaching maturity [7, 8].
The dominance of many marine juvenile fish in the Pangani mangrove estuary along with intense fishing practices raises concern about the abundance of resource base and how do predatory fish species with similar feeding habits, partition dietary resources and thus, manage to co-exist. The presence of species that occupy the same trophic level and demonstrate similar trophic niches in such a highly disturbed estuary can be an indication of the stability of the food web structure . This is frequently related to the occurrence of predatory fish with trophic linkages originating from diverse trophic base resources [9, 10]. Under such circumstances, loss of connectivity within and across trophic levels is unlikely to occur due to energy flow higher up the food web through multiple channels [6, 10]. Pelagic, benthopelagic and even benthic predatory fish are important to maintain the food web stability since they link pelagic and benthic food chains in aquatic ecosystems through feeding relationships [10, 11]. In addition, knowledge on the trophic interaction among autotrophs, primary consumers and predatory fish can help describe how these predators affect and depress the biomass of organisms down the food web. Studies on the trophic relationships of marine juvenile predators that link top predators and primary consumers are limited in estuarine systems [10, 12] particularly in Tanzania where estuaries are highly disturbed due to fishing.
Stable isotopes and stomach content analyses are methods that complement each other to gain more insight into the feeding relationships of fish species and the degree of dietary resources sharing in different aquatic systems [2, 6, 13, 14]. Integrating these two methods is important for the interpretation of feeding results. Through stomach content analysis, it is easier to determine what types of prey (at high taxonomic level) are instantly ingested by predators . However, the method does not allow the assessment of what types of prey have been historically assimilated by the species which is revealed by stable isotopes . Carbon and nitrogen isotope ratios reflect long-term diets  and quantify the primary food sources  assimilated by the species during the time the organism is growing. The use of stable isotopes is important, especially when characterizing the diet and feeding interaction of predatory fish species like groupers that have high prey regurgitation and stomach vacuity index . Due to the ability to integrate assimilated dietary signatures on a long-term basis and differentiate dietary sources of marine and fresh water origin, stable isotope analyses can better infer the nutritional sources and feeding relationships of juvenile marine predatory species throughout the period they spent in the estuarine nursery ground.
Juvenile marine fish are currently dominating fish assemblages in the Pangani estuarine system. This has resulted by the increasingly inland intrusion of sea water through tidal actions as a consequence of reduction in fresh water inflow into the estuary [19–21]. The predatory marine fish species present in the estuary among others, include lutjanidae (e.g. Lutjanus argentimaculatus), sphyraenidae (e.g. Sphyraena jello), hemiramphidae (e.g. Hyporhamphus dussumieri), gobiidae, serranidae (e.g. Epinephelus species), carangidae (e.g. Carangoides species) and others . These species differ in salinity tolerance along the salinity gradient, as well as feeding habitats and area within the water column . The feeding of some fish species is directly or indirectly connected with the mangrove habitats. Few marine predatory species are abundant in the upper Pangani estuarine zone where the banks of the estuary are fringed with coconut palm trees. Lower and middle estuarine zones are dominated by mangrove forest . Greasy grouper or black-spot estuary cod, Epinephelus malabaricus and longnose trevally, Carangoides chrysophrys, are abundant predator species in estuaries at juvenile and sub-adult stages [7, 23, 25, 26]. In the Pangani estuary, they are abundant in the lower, middle and upper or innermost zone from the estuary mouth. They are among the multiple fish caught by local fishermen throughout the Pangani estuarine zone. Unfortunately, no documented data are available for the movement, feeding pattern and other ecological features of these species in Tanzanian estuaries . A study conducted by Bhat et al.  in the Aghanashini estuary, in India indicated that C. chrysophrys was abundant throughout the year and across the estuarine reaches with average salinity ranging from 6.5 ppt (inner estuary) to 22.5 ppt (near estuary mouth).
Like other groupers which are slow growing, juvenile E. malabaricus use estuaries and other shallow habitats over a year and after reaching sexual maturity they migrate to deeper waters for spawning . This grouper is a protogynous hermaphrodite . Therefore, uncontrolled fishing of pre-mature individuals in the Pangani estuary can interfere with the reproduction cycle of the species. This grouper is also a voracious predator, feeding on fish, macro-crustaceans and in some cases even on octopuses. The species uses a sit and wait, ambush hunting style foraging behavior, and it is tolerant to low salinity and turbid environment . The species is in the list of near-threatened species as mentioned in the International Union for Conservation of Nature (IUCN) Red List . Likewise, C. chrysophrys, despite being a fast swimmer roving in nature, juvenile and sub-adults tend to spend a certain period of their time in estuaries and other coastal shallow water habitats and move out as they grow [25, 28]. Males of C. chrysophrys attain sexual maturity at 46.90 cm in length and females at 42.08 cm . The duration of stay of C. chrysophrys in the estuaries is not well known but literature indicates that it takes more than 2 years to reach maturity [25, 26]. Previous studies show that both species can compete for the dietary resources in estuaries as they consume small fish and epibenthic crustaceans including shrimps and crabs [25, 26, 28–31]. The high artisanal fishing pressure in the Pangani estuary with multiple catches including all available predatory fish species poses a need to identify the trophic niches and relationships of C. chrysophrys and E. malabaricus. These two species share trophic resources and feeding grounds, in particular, in the Pangani shallow estuarine system.
Therefore, the present study aimed at characterizing the trophic relationships between the juvenile co-existing predatory species, C. chrysophrys and E. malabaricus throughout the Pangani estuarine system by using stomach contents and stable isotopes of carbon and nitrogen. Specifically, the study focused on: (1) describing the main dietary composition in these species and their level of variation (2) assessing their sources of nutrition in a longitudinal salinity gradient in order to better explain their level of similarity/differences in trophic niches, (3) assessing their isotopic niches. The study answered the following questions: To what extent do the diets of these two species differ along the longitudinal estuarine salinity gradient? Do their sources of nutrition differ and to what extent? How do their trophic niches differ? Answering these questions will highlight the degree of the species connectivity to various trophic bases and resource partitioning, which is essential information when evaluating the estuarine community structure over time.
Field sample collection
Two predatory marine fish, C. chrysophrys and E. malabaricus and their potential preys and autotrophic sources were collected separately in the three sampling zones. Predatory fish and potential prey fish were caught by using seine net and monofilament gill nets of multiple mesh sizes at spring tides in October 2014, January, March, May and July 2015. The prey fish caught were dominated by clupeids (Hilsa kelee) and mugilids (Valamugil buchanani). After retrieval of the nets, prey fish and various sizes of the targeted predatory species, were selected and stored in a cool box with dry ice. Later on, wet weight (to the nearest 0.1 g) and total length (to the nearest 0.1 cm) were recorded, and predatory fish stomachs were removed and labeled. All fish samples and stomachs were frozen at − 20 °C on the same day. Overall, 135 samples of C. chrysophrys and 164 samples of E. malabaricus were collected and preserved for stomach contents analysis. For the prey fish, 64 samples of Mugilids and 59 samples of Clupeids were preserved for stable isotope analysis.
Along with fish sampling potential prey, invertebrates and autotrophs, were collected for stable isotope analysis. The fiddler and swimming crabs, gastropods and bivalves were collected by hand in the intertidal areas during low tides. Shrimps, dominated by Fenneropenaeus indicus and palaemonidae, Sesarma species and Scylla serrata crabs were obtained from fishermen at the time of retrieving their nets in each zone. Isopods were collected from barnacle shells. Amphipods were collected by a hand corer in shallow waters. The sediment cores were sieved through a 250 μm sieve, and the retained organisms were sorted, collected into containers and stored in a cool box. Three replicates of surface sediment were collected in shallow waters by using a cylindrical hand corer and the top 5 cm layer was removed and frozen for isotope analysis of surface particulate organic matter (sPOM). Microphytobenthos were collected by taking the top surface sediment layer (1 cm), using a hand corer in the unvegetated intertidal area, which was mixed with distilled water and filtered through a 63 µm sieve. The supernatant was incubated with pre-treated sand (acid washed and combusted) and then illuminated for 7 h, a process that facilitates microalgae to be phototactically attracted to the surface top layer of the sand. Separation of microphytobenthos from sand was done through treating the mixture with distilled water, and filtering again through a 63 µm sieve and a GF/F glass fibre . Samples of periphyton were collected by scraping rocks and fallen trees using a metal spatula. Macro-algae (green filamentous algae and Sargassum species) and sea grasses were also collected by hand. Leaves of mangrove trees Avicennia marina, Rhizophora mucronata, Bruguiera gymnorrhiza, Ceriops tagal, Sonneratia alba, Heritiera littoralis and Xylocarpus granatum were picked from tree branches only in the middle and lower estuarine zones; they were absent in the upper zone. Angiosperm (C3 and C4) plants including water hyacinth samples, palm leaves and Poaceae family grasses were picked by hand in the intertidal zone of the upper and middle estuary zones. All specimens after collection were bagged separately, stored in a cool box with dry ice in the field and later preserved in a freezer at − 20 °C in the laboratory.
Stomach content analysis
At the laboratory, fish stomachs were thawed, the contents were rinsed with distilled water and were examined under a compound microscope. The food items were identified to the lowest possible taxonomic level. The identified diet items were counted and weighed to the nearest gram according to Hyslop . The diet items were grouped into broader categories, namely brachyuran crab, mature penaeid shrimps, juvenile shrimps (post larvae and juvenile stages of all shrimp species), other shrimps (other mature shrimps), stomatopods, Teleostei (identified to family level) and digested materials. To determine the importance of each food item in the diet of each predatory fish species, the percent of prey-specific index of relative importance (%PSIRI)  was used. According to Brown et al. , %PSIRI is calculated using the following equation, %PSIRI = (%FOi (%PNi + %PWi))/0.5, where %FOi is the percent frequency of occurrence (the number of stomachs containing prey i divided by the total number of stomachs with food); and %PNi and %PWi are the percent prey-specific abundances by number and weight respectively. The percent prey-specific abundances are the average percentage abundance of prey i by number (%PNi) or weight (%PWi). Overall interspecific variation in the diet of the fish species across the three estuarine zones, intraspecific variations of the diet at a spatial scale and in different size classes were assessed by main and pairwise permutational multivariate analysis of variance (PERMANOVA). In order to test whether the species exhibit ontogenetic changes in diet, the dietary data of successive 5 cm length classes of each species in each estuarine zone were used. The PERMANOVA tests were run based on the Bray–Curtis similarity matrices made from the square root transformed weight percentage dietary data. PRIMERv6  with PERMANOVA + add-on module statistical packages  were used in these analyses.
Stable isotope analysis
The dorsal white muscle tissues from 58 samples of C. chrysophrys and 60 samples of E. malabaricus collected in January and March 2015 were prepared for stable isotope analyses. The pieces of the dorsal muscle from individual fish were washed with distilled water and sun-dried. Thereafter, the samples were ground into fine-powder, packed into airtight plastic vials and kept in a desiccator until the time of analysis. Invertebrates, soon after being thawed, were sorted (under a dissection microscope) into various taxonomic groups and washed with distilled water. For large invertebrates, tissue samples were collected from the various body parts including the abdominal muscles of decapod shrimps, the claws of brachyura, the muscular foot of gastropods and the adductor muscle of bivalves. For amphipods and isopods individuals were pooled, sun-dried, ground into powder and packed for stable isotope analyses. For the sPOM, the top centimeter of the sediment was separated from the frozen core and prepared for isotopic analysis. The microphytobenthos samples and other autotroph samples were unfrozen and prepared for isotopic analyses. All samples prepared were then sent to the Iso-Analytical Laboratory in United Kingdom for stable isotope analysis.
The relative proportion contributions of all autotrophs to the nutrition of fish in each estuarine zone were estimated using the isotope mixing model Stable Isotope Analysis in R package (SIAR) version 3.3.0 . More than one category of potential autotrophs with similar isotopic composition were combined as the model does not fit well when the isotopic values of food sources do not differ . The trophic position of consumer is important when running the model , thus the estimated trophic levels (TL) of about 3.0 for the C. chrysophrys and 3.2 for the E. malabaricus were used. These TLs were estimated following the method of Post  using Uca species, the primary consumer invertebrate as the baseline. Uca crabs (family Ocypodidae) were selected in this case because they were abundantly caught in all three sampling zones and largely feed on benthic algae and diatoms [43, 44]. The formula used was TLi = 2 + (δ15Ni − δ15NTbase/3.0) where: TLi = trophic level of fish species i, δ15Ni = is the mean nitrogen isotopic value for fish species i, δ15NTbase = mean nitrogen isotopic value of Uca species that was considered as trophic level 2 in each sampling zone. The trophic fractionation factors (TFF) of consumers used were 0.5 for δ13C and 3.0 for δ15N following the recommendation of Abrantes et al. , McCutchan et al.  and Vanderklift and Ponsard .
The Bayesian mixing models were also used to quantify the contributions of various preys to the diet of the predatory fish species. The stomach content analyses and available literature were used to identify the potential prey food sources that were preyed upon. The models were run separately for each estuarine zone by using the isotopic values of the predatory fish and their potential prey collected in the three respective zones. Also, before running the model, the δ13C and δ15N of the predatory fish were corrected for trophic fractionations using the same TFF values as applied above. The outputs of the model for each category of autotrophic and prey contributions to each fish species were presented as mode with 95% credibility interval for variance as recommended by Parnell et al. .
The Layman metrics mainly used to describe the trophic structure and trophic niches [47, 48] were calculated using Stable Isotope Bayesian Ellipses in R (SIBER) packages version 4.4 . These metrics among others were the range of δ13C values (CR) for measuring trophic diversity of the basal resources, standard ellipse area (SEA) and total area (TA). The TA represented by convex hulls is used to estimate the isotopic niche width of each fish species and their degree of resources segregation in sampling zones. The calculated standard ellipse areas in δ13C–δ15N bi-plot space, corrected for small sample size (SEAc) (n > 30) represented the bivariate standard deviation of the data and encompassed about 40% of the data . Convex hull area (TA) included all samples of each species in the δ13C–δ15N space, represents the total niche space occupied by the group. For statistical testing of the isotopic niche width of fish species, Bayesian standard ellipse area (SEAb) were estimated . Both SEAc and the estimated SEAb (after fitting Bayesian multivariate normal distributions to each species in the dataset) measure the feeding niches and indicate the degree of niche overlap among the species. Both SEAc, SEAb are unbiased with respect to sample size and display more uncertainty with smaller sample size [48, 49].
Diet composition of Carangoides chrysophrys and Epinephelus malabaricus from the Pangani Estuary
Total empty stomachs (%)
Total stomachs with food (%)
Prey-specific index of relative importance (%PSIRI) for the predatory fish in the Pangani estuarine zones
The two ways PERMANOVA revealed the high level of variation in the diets between C. chrysophrys and E. malabaricus across the three estuarine zones (p = 0.001, pseudo-F = 15.81) but it did not show any interaction between the species and sampling zones (p > 0.05; pseudo-F = 0.43). Lack of interaction for the fish species and estuarine zones factors, was further shown by the pair-wise PERMANOVA tests which indicated no spatial intra-specific diet variation of both species for each pair of zonal comparison (p > 0.05; t ≤ 1.07). With respect to fish size, one-way PERMANOVA confirmed that the two species did not show a significant shift in diet as they grew throughout the estuarine zones (p > 0.05).
Stable isotopes of autotrophic sources
Stable isotopes of autotrophic sources (mean ‰ ± standard deviation) in Pangani estuary
Primary food source
Upper estuarine zone
Middle estuarine zone
Lower estuarine zone
− 23.9 ± 0.7 (3)
6.8 ± 0.2 (3)
− 23.3 ± 0.5 (3)
6.9 ± 0.2 (3)
− 22.9 ± 0.7 (3)
6.4 ± 0.3 (3)
− 23.4 ± 0.3 (3)
5.4 ± 0.4 (3)
− 22.75 (2)
− 19.9 (2)
− 20.6 (1)
− 20.5 (1)
− 20.2 (1)
Filamentous green algae
− 22.0 (2)
− 21.6 ± 1.4 (4)
6.1 ± 0.3 (4)
Macro-algae (Sargassum sp.)
− 16.8 (2)
− 13.7 ± 1.0 (3)
4.0 ± 0.2 (3)
− 12.9 ± 0.3 (5)
5.2 ± 1.2 (5)
C3 Mangrove plant
− 28.4 ± 1.2 (8)
5.4 ± 1.8 (8)
− 28.7 ± 0.8 (7)
3.9 ± 1.9 (7)
− 28.1 ± 1.3 (5)
6.5 ± 2.5 (5)
− 27.9 (1)
Stable isotopes of fish and potential prey
Stable isotopes of invertebrates and fish studied (mean ‰ ± standard deviation) in the Pangani estuary
Upper estuarine zone
Middle estuarine zone
Lower estuarine zone
− 18.1 ± 1.2 (5)
8.9 ± 0.5 (5)
− 16.8 ± 0.3 (4)
8.6 ± 0.5 (4)
− 20.1 ± 2.3 (6)
7.0 ± 1.1 (6)
− 18.2 ± 2.4 (3)
6.7 ± 0.3(3)
− 17.3 (2)
− 18.9 (2)
− 18.1 (2)
− 20.9 (1)
− 19.6 (1)
− 18.4 (1)
− 19.6 ± 1.9 (7)
10.2 ± 0.5 (7)
− 18.6 ± 1.5 (9)
9.8 ± 0.8 (9)
− 18.5 ± 1.7 (8)
9.8 ± 0.6 (8)
Penaid and palaemonid shrimps
− 20.2 ± 1.1 (6)
10.5 ± 0.7 (6)
− 20.7 ± 0.8 (4)
10.6 ± 0.4 (4)
− 18.9 ± 0.5 (5)
10.4 ± 0.6 (5)
− 17.8 ± 0.6 (19)
10.8 ± 0.4 (19)
− 17.8 ± 0.5 (20)
11.1 ± 0.7 (20)
− 17.6 ± 0.5 (20)
10.9 ± 0.5 (20)
− 23.2 ± 0.7 (20)
13.0 ± 0.5 (20)
− 22.8 ± 1.0 (22)
12.8 ± 0.7 (22)
− 22.3 ± 0.8 (22)
12.4 ± 0.8 (22)
− 19.7 ± 0.9 (19)a,*
13.5 ± 0.5 (19)a,*
− 19.3 ± 1.1 (20)ab,*
13.5 ± 0.5 (20)a,*
− 18.9 ± 1.1 (19)b,*
13.3 ± 0.5 (19)a,*
− 19.1 ± 1.0 (21)a,*
14.0 ± 0.9 (21)a,**
− 18.8 ± 0.8 (19)a,*
13.9 ± 0.6 (19)a,**
− 17.5 ± 0.6 (20)b,**
13.9 ± 0.4 (20)a,**
The ANOVA results revealed that the δ13C values of C. chrysophrys and E. malabaricus were significantly different in the middle and lower portions of the estuary but not in the upper estuarine zone (Table 4). The δ15N of both species were statistically different in all three estuarine zones (Table 4). Across the estuarine zones, each fish species displayed insignificant changes in δ15N ratio (ANOVA, p > 0.05). The δ13C values of C. chrysophrys were slightly different between samples caught from the upper and lower estuarine reaches (ANOVA, F = 5.86, p < 0.05) but similar in δ13C ratio of samples caught in the other two possible zonal comparisons. The δ13C ratio of E. malabaricus slightly increased with increasing distance from the upper estuarine reaches towards the estuary mouth (Table 4). The δ13C values of this species were different between the upper and lower zone (ANOVA, F = 43.37, p < 0.001), as well as the middle and lower part of the estuary (ANOVA, F = 33.7, p < 0.001). For the pooled estuarine zonal δ13C and δ15N data, the two predatory fish species were isotopically distinct (ANOVA, F ≤ 19.9, p = 0.0001).
The linear regression results for the pooled isotopic data across the estuarine zones, showed no significant relationship between fish length and δ13C or δ15N ratios of C. chrysophrys (F1, 53 ≤ 0.92, r2 ≤ 0.02, p > 0.05). For E. malabaricus, the linear regression of the combined estuarine zonal data revealed no significant relationship between fish size and δ15N (F1, 58 = 1.3, r2 = 0.02, p > 0.05). However, E. malabaricus exhibited a weak positive linear relationship between length and δ13C values (F1, 58 = 5.0, r2 = 0.08, p = 0.03). Regarding the linear regression results of each species in every estuarine zone, it was found that both species had no relationship of fish size and δ13C or δ15N values (F ≤ 4.2, r2 ≤ 0.2, p > 0.05).
Autotrophic sources supporting the nutrition of fish
In the middle part of the estuary, microphytobenthos were again the main autotrophic sources, and their percent contributions were slightly higher [C. chrysophrys (56–76% CI), E. malabaricus (54–75% CI)] when compared to those from the upper part of the estuary (Fig. 2). The second most important food source assimilated by both species were C4 grasses but the percent contribution were slightly lower than that revealed in the upper estuarine zone (Fig. 2). sPOM, periphyton, filamentous green algae and C3 plants were less important (Fig. 2). In the estuarine mouth zone, seagrasses and macro-algae (Sargassum species) were the key food sources for C. chrysophrys and E. malabaricus (21–55% CI and 29–60% CI, respectively). The next important food source were C3 plants for both C. chrysophrys and E. malabaricus (Fig. 2). Microphytobenthos indicated the broader percent contribution to the nutrition of both fish species in the lower portion of the estuary. However their importance were slightly lower when compared with their position in the other sampling zones, as their credible contribution lay between 0% to about 55% (Fig. 2).
Important prey supporting the nutrition of fish
Proportional contributions of food items for C. chrysophrys and E. malabaricus in Pangani estuary
Upper estuarine zone
Middle estuarine zone
Lower estuarine zone
Caridea and penaeidae shrimps
Upper estuarine zone
Middle estuarine zone
Lower estuarine zone
Caridea and penaeidae shrimps
Trophic niche characteristics of fish
Isotopic niche data of Carangoides chrysophrys and Epinephelus malabaricus in the Pangani estuarine zones
Isotopic niche data
Upper estuarine zone
Middle estuarine zone
Lower estuarine zone
SEAb (mean ‰2 ± SD)
1.35 ± 0.37
2.51 ± 0.32
1.64 ± 0.56
1.13 ± 0.17
2.06 ± 0.50
0.72 ± 0.19
The isotopic mixing models and dietary results revealed that the high-speed swimming and roving C. chrysophrys and the less mobile E. malabaricus consumed similar types of prey but in different proportions, in the various reaches of the Pangani estuarine system. The isotopic mixing models also verified that the two species differ in the isotopic niche width they occupy, across the longitudinal estuary gradient. Differences in the amount of prey consumed are likely to be justified by prey distribution in the feeding habitats (i.e., benthic and benthopelagic), prey catchability, feeding strategies and energy requirements of each species [12, 50]. Because of the high swimming speed laterally and longitudinally, C. chrysophrys is capable of capturing highly mobile prey that are abundant all over the water column, whereas, the sedentary nature and ambush foraging strategy of the benthic E. malabaricus [7, 26, 31, 51] enables it to capture large amounts of less mobile zoobenthos.
The differences in foraging habitats (defined by depth) and foraging strategy of these two predatory fish species, typifies the lower δ13C values of C. chrysophrys when compared to that of E. malabaricus in all three estuarine zones. It is known that the mid-water and pelagic food sources tend to display more negative δ13C ratios whereas, the benthic food sources exhibit less negative δ13C ratio . Thus, the interspecific variation in δ13C values probably resulted from the fact that C. chrysophrys depends on the mid-water and pelagic prey in addition to benthic, which is reflected in the more negative δ13C values compared to the mostly benthic (and less negative δ13C) signal of E. malabaricus. It was, however, noted that the most important preys consumed by the two species as revealed by the dietary indices, were to some extent different from the most assimilated prey by the same species, as shown by isotopic mixing models. The overemphasized prey category of brachyura and shrimps as indicated by stomach content analysis over small bony fish revealed by isotopic mixing models suggests that either the two species rely on prey types whose abundance vary greatly, or these prey types share similar basal nutritional sources that were not affected by season. Such justifications are supported by the long-term, isotopic signal dietary tracers that reveal diets consumed by the species for the past 3 months. More so, the high occurrence of large sized preys like brachyura in the diet of E. malabaricus in contrast to numerous juvenile shrimps predated by C. chrysophrys could be correlated to differences in their mouth morphology [30, 53].
The varied δ13C values of E. malabaricus across the estuarine zones further demonstrates that the feeding of this species is site-specific and localized due to a limited foraging movement among the estuarine zones [54, 55]. Moreover, the differences in the prey foraging strategies of C. chrysophrys and E. malabaricus may have contributed to the interspecific differences in δ13C and δ15N signatures, indicating trophic niche differentiation and co-existence in the estuary. The difference in the percent contributions of mugilids and clupeids to the nutrition of C. chrysophrys and E. malabaricus suggests that these species differ in the trophic pathways of acquiring their carbon sources and nutrients. This is because mugilids form the component of the benthic food web; and clupeid the component of the planktonic food web. Provided that these predatory fish species showed different proportions of relying on mugilid and clupeid diet, they exploit differently nutrients and energy channels from pelagic and benthic food webs. This situation reduces fragility and increases trophic connectivity of estuarine food web structure [9, 10].
Furthermore, the findings suggest that there could be a facultative mutualistic feeding interaction between C. chrysophrys and E. malabaricus. This means that the high speed, patrolling technique of seizing preys on the bottom of the sediment by C. chrysophrys tends to disturb the epibenthic organisms like gobies, shrimps and brachyura. Such disturbance predisposes these prey items to be readily caught by E. malabaricus, a predator that seizes its prey through sit-and-wait ambush strategy. Apart from that, the low salinity portion of the estuary which is more turbid and structurally complex, probably enhances the prey-capture success by E. malabaricus. The structurally complex habitat provide enhanced cover that reduces the possibilities of predators to be detected by the preys . This situation is perhaps connected with the observed broader isotopic niche space of E. malabaricus when compared to that of C. chrysophrys in the upper estuarine zone. The catchability of prey by C. chrysophrys is likely to be affected by the turbid conditions which lowers its visibility  in the upper estuarine zone.
The observed changes in the main autotrophic sources C. chrysophrys and E. malabaricus relied on in the three estuarine zones, could be underpinned by the selectivity of the trophic basal sources by organisms that are preyed on by predatory fish. Selectivity of the autotrophic resources by primary consumers is largely driven by digestibility of the resources. According to Mann  and Dias et al.  terrestrial C3 and C4 plant food sources are refractory, less labile relative to micro- and macro-algae food sources. The reliance on sea grass and macro-algae (Sargassum species) by C. chrysophrys and E. malabaricus in the lower sampling zone, indicates that their preys most probably feed on and assimilate the autotrophic source that is readily abundant. Matich et al.  also observed that Carangoides species and other coastal predatory species in northern Tanzania reflected the isotopic signals of the mixed algae and sea grasses due to the high abundance of these autotrophic sources.
Notably, the Panagni estuary is shallow  with wide intertidal mudflat that supports microphytobenthic production [59, 60] while marine microalgae are washed into the estuary by strong tidal flows. This is probably reinforced by the reduced freshwater flow due to water use for three hydro-electric power generation, and water abstraction for irrigation schemes upstream the Pangani River catchment [19, 20]. On the other hand, the δ13C values representing C4 plant as the second most assimilated autotrophs by fish species in the upper and middle zones, are likely to be a combination of the isotopic signals derived from both C4 plant and sea grasses from the lower part of the estuary. This is due to the fact that the δ13C values of these two autotrophs are relatively similar. This has an implication to the isotopic signals of the non-stationary C. chrysophrys and preys such as clupeids, engraulids and shrimps that frequently and unlimitedly move across the estuarine zones. This situation can also confirm the limitation of using isotopic values for the study of the dietary sources of estuarine consumers at fine spatial scales.
Unlike E. malabaricus, the decreasing trends of niche breadth (measured by carbon isotopic range) and isotopic niches of C. chrysophrys from the lower zone towards the upper estuarine zone, further highlight that, the two species differ in salinity and turbidity tolerances accompanying their feeding habitats. These trends suggest that C. chrysophrys migrates to the middle and upper estuarine zones to avoid high risk of predation and other anthropogenic disturbances that is common along the coast and township of Pangani. On the other hand, the larger isotopic overlapping space in the middle zone relative to that of the upper and lower estuarine zone is probably due to potential inter-specific competition. Because of potential inter-specific competition in the middle zone, the fish species can easily move out of that zone to either the upper or lower zones to reduce competition. This situation is probably linked with the broader isotopic niche of E. malabaricus in the upper estuarine reaches, which is the result of the species escaping potential competition in the middle zone and disturbances in the lower estuarine zone.
The dominance of benthic estuarine and marine microalgae in the nutrition of the fish species is probably an indication that there are lower connectivity options between the estuarine nursery food webs and the terrestrial or freshwater food webs. In this case, fragmentation of the food web is likely to occur, a situation which reduces the ecosystem complexity while weakening the preliminary nursery function of the estuaries. The situation is intensified by increasing anthropogenic fresh water use upstream of the estuary, as well as disturbances related to the local fishermen that frequently use the estuary as a fishing ground. Thus, the responsible authorities of the Pangani River Basin are advised to manage, and thus reduce all anthropogenic activities that are currently threatening the estuarine ecosystem.
The present study also demonstrates that not all estuarine benthic predatory fish communities and their prey, reflect the estuary gradient difference in δ13C signals of primary food sources . Instead, this depends on the distance in between the sampling points and the foraging movement pattern of the animals. As for the case of δ13C ratio of the high mobile C. chrysophrys, our findings concurred with the study by Selleslagh et al.  who revealed that within the fine scale estuarine sampling points, no significant isotopic differences can be detected. Moreover, only site fidelity juvenile predatory fish species such as E. malabaricus  are able to show the isotopic signals similar to that of the basal nutritional sources found in the habitats the species is caught . Likewise, our isotopic results displayed similar patterns reported by Claudino et al.  who emphasized that some fish and decapod invertebrates incorporate the most abundant autotrophic sources in habitats they occur. Claudino et al.  further showed that consumers near the estuary mouth, acquire their nutrients derived from macro-algae and seagrass, in contrast to the consumers from the upper estuarine zone that accumulate their nutrients from mangrove and macro-algae.
The study described how the two juvenile predatory species, C. chrysophrys and E. malabaricus were spatially and trophically connected to each other, despite differences in their positions when feeding in the water column of the Pangani estuarine system. It was revealed that both species consume small fish, shrimps and brachyura constituting similar and narrow trophic resources base. The differences in their diets relied on the proportions of each prey consumed by individual species. The species differed significantly in their isotopic trophic niches but with considerable dietary overlap. The spatial inter-specific differences in isotopic trophic niches across the longitudinal estuary gradient were revealed by the presence of autotrophic sources that were isotopically distinct among the estuarine zones.
Nevertheless, the isotopic models confirmed that clupeid species feeding in the water column and mugilids feeding in the surface sediment were the main intermediate prey linking predatory fish species to the main autotrophic sources, microphytobenthos, sea grass and macro-algae. This suggested that the benthic predatory species in the Pangani estuarine system are trophically linked with both planktonic and benthic components of the estuarine and marine food web but not that of the fresh water food web. Similarly, the reliance on estuarine and marine related basal food sources of the predatory species, reduces the connectivity of terrestrial and estuarine food webs, a situation that threatens the stability of fish nursery food web structures. Susceptibility of estuarine food web structures would increase especially when the high rate of removal of meso predatory species will keep on increasing. This would result in the reduction of trophic connectivity and complexity, the indicators of low resilience ecosystem upon any disturbances. More studies and monitoring of all species caught by fishermen and the trophic relationship with other food web compartments will enhance our understanding of human impacts on the ecosystem in question and thus, improve the management strategies of estuarine and coastal ecosystems.
APM performed the study design, field sampling, laboratory sample preparation, data analysis and manuscript writing. DAS participated in laboratory data analysis, supervised study design, the data analysis, manuscript preparation and selection of target journal for publication. JFM provided the supervision of study design, field sampling and writing the manuscript. All authors read and approved the final manuscript.
The authors are grateful to the technical support and research facilities provided by the University of Dar es Salaam, College of Agricultural Sciences and Fisheries Technology. Authors appreciate the support of Dr. Martin Genner (from University of Bristol) and Dr. Benjamin Ngatunga (Ichthylogist) that agreed to handle transportation of samples to Iso-Analytical Laboratory in United Kingdom and funding part of stable isotope laboratory data analysis.
The authors declare that they have no competing interests.
Availability of data and materials
The most data generated during the current study are included in this manuscript, only dietary related data will be available from the corresponding author during the process of reviewing the manuscript.
Consent for publication
Ethics approval and consent to participate
Since the study was part of the PhD thesis, the study was carried out in accordance with the Tanzania law and University of Dar es Salaam guidelines for collecting and handling plant and fish related data. All procedures related to this study were approved by the Committee of the College of Aquatic Sciences and Fisheries Technology of the University of Dar es Salaam.
The study was mainly funded by the Tanzania Commission for Science and Technology (COSTECH) that covered the study design, data collection and interpretation of the results.
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