ARTICLE

Diet and isotopic metrics of predatory and prey fish in two estuaries
with different degrees of anthropogenic disturbances:
the case study of Wami and Pangani rivers in Tanzania
Theresia John Lyasenga1, Alistidia P. Mwijage2, Dativa Joseph Shilla3, John Andrew Marco Mahugija4, Lydia Gaspare1,
Daniel Abel Shilla1, Prosper Laurent Mfilinge1
1
School of Aquatic Sciences and Fisheries Technology, University of Dar es Salaam; 2Tanzania Fisheries Research Institute (TAFIRI),
Dar es Salaam; 3Department of Chemistry, Dar es Salaam University of College of Education (DUCE); 4College of Natural and Applied
Sciences, Department of Chemistry, University of Dar es Salaam, Tanzania

ABSTRACT
Diverse anthropogenic activities including alteration of hydrological regime and agricultural development in the upstream of
the river catchments modify the structural components of communities and ecological roles of species in estuarine ecosystems.
The present study compared the diet, carbon (δ13C) and nitrogen (δ15N) isotope ratios and Layman community metrics of predatory
fish and their prey-fish between two estuaries with different degrees of anthropogenic disturbances. The Layman community metrics
were estimated following the Bayesian approach. It was revealed that the diets of the predators Arius africanus, Epinephelus

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coioides, Sillago sihama and Pomadasys argenteus, and their isotopic values including their main prey, the fish Valamugil

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buchanani, were significantly different between Wami and Pangani estuaries (PERMANOVA, Pseudo-F≥3.1, p=0.05). The com-
parison test of isotopic niche width at estuary level showed that the isotopic niche of Wami estuary was slightly narrower (3.90-
6.94 at 95% CI) than that of Pangani (5.70-9.69 of 95% CI). The comparison of the δ15N values and range of species between

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estuaries suggest shifts in trophic position of the species in Wami estuary relative to that of Pangani. Furthermore, the Layman
metric indices of trophic diversity and redundancy of Wami estuary were substantially smaller, when compared to that of Pangani
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estuary. These findings indicate that, even though the Wami estuary stands under a conservation status, the extent of disturbances
in the upstream is potentially high and enough to induce the ecological changes at the base of the food web downstream, giving
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rise to subsequent effects transmitted to higher-order consumers. As a result, the ecological redundancy and ecosystem complexity
of Wami are possibly compromised relative to that of Pangani estuary.
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fluctuations are hydrological regimes, encompassing

INTRODUCTION freshwater discharges from the upstream, coastal wave ac-
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Estuaries are among the most biologically productive tivity and tidal water flow at the mouths of the estuaries
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and economically valuable ecosystems in the world. The (Gillson, 2011; Hoeinghaus et al., 2011). The interference
hydrological regime and geomorphological features of es- of such hydrological regime such as upstream water ab-
tuaries make such ecosystems good shelters, feeding and straction for irrigation and damming for hydropower gen-
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breeding grounds for many marine fish species at various eration causes retention and thus reduction of nutrients,
stages of their life cycles (Beck et al., 2001; Pihl et al., sediment (that serve as an ecological niche to some
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2002; Harrison and Whitfield, 2006; Kostecki et al., 2010; species), quantity and quality of organic matter reaching
Selleslagh et al., 2015). Estuaries provide essential and the estuary (Han et al., 2016). Variations in the hydrolog-
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complex habitats to sustain different freshwater and ma- ical regime impact habitat availability and diversity, pri-
rine fish stocks. The estuarine complexity provides juve- mary production, trophic interactions and consequently
nile fishes with adequate protection from predation while prompt responses in food web structure and functioning
attaining high growth rates supported by a high primary (Gillson, 2011; Whitfield, 2016; Donázar-Aramendía et
productivity (Kostecki et al., 2010; Whitfield, 2016). Nev- al., 2019). More so, the regulation of the flow rate of
ertheless, the ecological status of most estuaries is threat- freshwater reaching the estuaries greatly influences the
ened due to modifications made by anthropogenic diversity of basal organic matter fueling the estuarine food
activities. Estuaries are subjected to increasing human webs (Abrantes et al., 2013).
pressure through urbanization, overfishing and upstream Juvenile marine fish with predatory behavior constitute
catchment disturbances resulting from deforestation, a great part of estuarine fish communities. They are highly
water abstraction for reservoir or multi-dams construction targeted by local or artisanal fisheries while still at juvenile
and water diversion for irrigation activities (Abrantes et and sub-adult stages, as they attain large body sizes before
al., 2014). reaching maturity (Shaw et al., 2016; Mwijage et al.,
The physical, chemical and biological characteristics 2018a). As such, they have lucrative market price when
of estuaries are dynamic both on temporal and spatial compared to the small fish that feed at lower trophic levels.
scales (Selleslagh et al., 2015). The main drivers of such Predatory fish and other higher order consumers coexist
84 T.J. Lyasenga et al.

in estuaries as they exert reciprocally positive indirect ef- trophic structure in numerous ecosystems. Stable isotopes
fects by regulating the populations of their respective ratios of carbon (δ13C) and nitrogen δ15N can be used as a
preys, and in that way, prevent competitive exclusion of robust tool to evaluate changes in the diet of native species
each other’s preys (Sanders et al., 2018). They also link in relation to the expansion of invasive species (García et
pelagic, benthic and detritivore food webs in estuarine al., 2020). Stable isotopes are also used to analyze the
ecosystems through predator-prey interactions (Rooney trophic niche, dietary overlap and other trophic dynamics
and McCann, 2012). Because of the array of ecological of food web components across varied ecosystems (Lay-
roles they play, by studying these predators, one can get man et al., 2012; Jackson and Parnell, 2016; Gutmann and
insights into the role of predatory fish for maintaining the Britton, 2018; Wang et al., 2018; Zhang et al., 2019).
structure and functioning of estuarine ecosystem. Through the Bayesian framework, Layman metrics are es-
The Pangani and Wami River estuaries are situated timated to enable evaluation of the numerous human-in-
about 55 kilometers apart in the coastal northern part of duced impacts on food webs, including ecological
Tanzania. The Pangani estuary is managed by Pangani redundancy, resilience, diversity and trophic stability of
Water Basin Office Authority, and thus it is an open access ecosystems (Rooney and McCann, 2012; Matich et al.,
estuary. The Wami estuary is part of Saadani National 2017; Donázar-Aramendía et al., 2019).
Park (SANAPA) and is therefore a protected estuary but In this study, we examine the degree of dietary and
the whole river is managed by Wami-Ruvu Water Basin isotopic niche flexibility of predatory fish and their phyto-

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Office Authority. However, the upstream part of Pangani detritivore prey-fish in the adjacent estuaries of Wami and

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and Wami rivers are subjected to different anthropogenic Pangani rivers. Specifically, our study intended to (i) as-
activities that may be affecting the ecology of estuarine sess the extent of similarity or overlaps in diet of preda-
fish and other biota in different ways. In the upstream por- tory fish; ii) estimate isotopic values and trophic niche of

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tion of Pangani catchment, water is mainly abstracted by predatory fish and their phyto-detritivore prey-fish popu-
multi-damming for hydroelectric power generation and
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lations; and (iii) elucidate the status of complexity, re-
irrigation (Shaghude, 2016; Mwijage, et al., 2018a). The silience and redundancy of two estuarine ecosystems
retained sediments and organic particles in the reservoirs using Layman metrics. In presenting and discussing our
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and the elevated load of nutrient inputs arising from these results, we provide critical information to further under-
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activities affect different ecological processes downstream stand the effects of the anthropogenic activities on fish
the rivers including estuaries. Yet, water upstream of communities and the resulting impacts on the Tanzanian
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Wami estuary is widely used for fishing and irrigation in river ecosystems as well as refine management ap-
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rice paddies and commercial sugarcane plantations proaches for sustainability of riverine and coastal re-
(Eeden and Koppen, 2016). sources in general.
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There is an indication that the multi-damming activi-

ties in Pangani catchment have reduced the nutrients load-
ing downstream (Selemani et al., 2017) and caused some METHODS
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predatory fishes to largely rely on the estuarine and ma-

Study area
rine organic matter sources (Mwijage et al., 2018a). In the
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Wami estuary, the basal primary food sources sustaining The study sites were based in the two macro-tidal es-
the components of the estuarine food webs is unknown. tuaries of semi-diurnal type adjacent to each other, located
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Despite the fact that the Wami estuary receives elevated in the northern coastal part of Tanzania, namely, Wami
nutrients and suspended particles from the upstream, ac- and Pangani estuaries (Figure 1). Both estuaries are per-
cording to Kiwango et al. (2015), the estuary is still eco- manently open, connected to the sea. The Wami estuary
logically healthy. Generally, the anthropogenic is part of the Saadani National Park (SANAPA) which
disturbances of Tanzanian estuaries and coastal ecosystem was established in 2005 and thus, it is strictly protected.
is high (see, e.g., Semba et al., (2016) and Shaghude The tidal range in this estuary reaches up to 4 m during
(2016)), but little is known about the implications of such spring tides and the influence may extend up to 8 km up-
disturbances on the trophic niche, and other related dy- stream (Kiwango et al., 2018a). During the wet season,
namics, of fish assemblage and, consequently, on the en- the freshwater plume of Wami River extends for several
tire estuarine ecosystem. hundred meters into the Indian Ocean during both low and
This paper aims at getting more insight into the above- high tides. Only the first five kilometers from the shore
mentioned perspectives, by comparing the diet and other are occupied by mangroves. The estuary shows turbidity
trophic dynamics of fish species at the different degrees ≥400 NTU and suspended sediment concentrations of
of anthropogenic disturbances present in Wami and Pan- <100 mg L-1 during the dry season, and >800 mg L-1 dur-
gani estuaries. Stable isotopes and stomach content analy- ing the wet season (Kiwango et al., 2018a). A salt wedge
ses are employed in complementarity to describe the is common in the offshore areas of Wami, several hundred
 Estuarine fish trophic dynamics and anthropogenic disturbances 85

meters from the mouth of the river in a northeasterly di- dry-season month and within the peak of the southeast
rection. The Pangani estuary is located further north of monsoon. Thus, field sampling was conducted after the
Wami estuary (Figure 1) with a wave amplitude of about peak of the rainy season which usually occurs in May; this
3.5 m during the spring tides and 3.0 m at neap tides allowed to reduce seasonal biasness by capturing isotopic
(Mwijage et al., 2018a). The estuary extends to about 20 values that would reflect dietary sources that were con-
km from the estuary mouth (Mwijage et al., 2018a). It has sumed by fish during the wet and dry seasons. This is
an extensive mangrove forest interspaced with based on the premise that isotopic values of consumer tis-
coconut/palm trees. Pangani estuary experiences strong sues indicate their long-term assimilated diet of at least
mixing of fresh and saline water. The hydrological regime three months. Fish species were caught by using monofil-
is mainly regulated by the multi-reservoirs upstream of ament gill nets of multiple mesh sizes and seine net with
the catchment. Moreover, both estuaries serve as breeding the dimensions of 15 m length, 1.5 m width and mesh size
and nursery grounds for marine fish, prawns, and birds, 0.5 mm. From the total landing, five abundant predatory
and they are known as the most productive areas of fish species, namely Arius africanus (Günther 1867), Ep-
prawns for Tanzania. Wami estuary, to a larger extent, inephelus coioides (Hamilton, 1822), Sillago sihama
hosts a larger number of hippopotamus and crocodiles (Forsskål, 1775) and Pomadasys argenteus (Forsskål,
compared to those occurring in the Pangani estuary. 1775), and their main potential prey such as the phyto-de-
tritivore Valamugil buchanani (Bleeker, 1853), were se-

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Field sampling procedures of fish lected to study their trophic niches flexibility. The

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Fish samples were collected in Wami and Pangani selection was based on what predatory fish species of ma-
River estuaries in July 2019 during the daytime. July is a rine affinity are abundant throughout the seasons
(Bianchi, 1995; FIU-GLOWS, 2016).

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Notably, marine fish species inhabiting Wami estuary
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include A. africanus, V. buchanani, Chanos chanos, Am-
bassis gymnocephalus, Hilsa kelee, Thryssa spp., Leiog-
nathus equulu, Pomadasys spp., Epinephelus spp. and
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Tetraodontidae, (Anderson et al., 2007; FIU-GLOWS,

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2016). However, the diversity and abundance of these

species decrease sharply as the distance from the mouth
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of the river to the upstream increases (FIU-GLOWS,

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2016). In Pangani estuary, fish species with a marine ori-

gin commonly seen include C. chanos, A. gymnocephalus,
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Gerres filamentosus, V. buchanani, Lutjanus argentimac-

ulatus, sillago sihama, Epinephelus spp. and species from
the families of Sphyraenidae, Hemiramphidae, Gobiidae
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and Carangidae (PWBO/IUCN, 2008; Bianchi, 1995;

Mwijage et al., 2018a).
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During the sampling, the predatory fish species E.

coioides and A. africanus were caught in both estuaries
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along with their main prey, i.e., V. buchanani. Both S. si-

hama and P. argenteus were abundantly caught in Pangani
estuary, while P. argenteus was greatly caught within the
plume setting at short distance from the mouth of the
Wami estuary. Since the two above-mentioned species are
classified as zoobenthivore under the feeding mode func-
tional grouping (Elliott et al., 2007), their trophic require-
ments are equivalent. Due to that, we decided to select
them as another pair of comparison between estuaries. To
get enough samples for stomach content analysis, addi-
tional samples of P. argenteus were bought from the local
market immediately after being landed by local fisher-
men. All fish species caught were stored in ice boxes con-
taining dry ice immediately after collection. Later, total
Figure 1. Map of Wami and Pangani river estuaries showing the length and weight were recorded, and all fish samples
study area. frozen at -20°C on the same day and transported to the
86 T.J. Lyasenga et al.

laboratory at the University of Dar es Salaam, College of grams to measure the similarity in diet, and the PER-
Agricultural Sciences and Fisheries Technology for fur- MANOVA tests were run based on the Bray Curtis simi-
ther analyses. larity matrices made from the square root transformed
volumetric percentage dietary data using PRIMERv6 with
Fish stomach content analysis PERMANOVA + add-on module statistical packages (An-
derson et al., 2008). Before conducting any statistical test,
In the laboratory, stomachs of all fish species caught
diet data were subjected to normality and homogeneity of
were extracted and subjected to content analysis. The fish
variance tests, the assumptions were not met. Thus, non-
stomachs were dissected under a microscope to enable the
parametric method was opted and because of the multiple
determination of the frequency of occurrence (%FO) and
variables, the multivariate analyses of variance tests were
percentage volumetric contribution of each dietary item
selected.
to the total stomach volume (%V). This was done follow-
ing the point method described by Hyslop (1980). The diet
Stable isotopes and trophic niche indices analyses
items were identified at the possible low taxonomic level.
Each food content in the stomach was allotted one of the For each fish species collected for stomach content
number of points - 0, 1, 2, 4, 8 and 16 - based on its vol- analysis, representative samples were selected randomly to
ume, from the smallest to the largest value, respectively. extract dorsal white muscle tissues for stable isotope analy-
sis (SIA). The sample size (n) and length size (total length

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Then percentage volumes within each stomach analyzed
were then calculated to give the percentage composition - TL - in cm) of each species were different: A. africanus

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in a diet of individual fish species. Also, vacuity index or from Wami = TL ranged 16.6-29.9 cm (n=16); A. africanus
the stomach emptiness index (VI) of each species was es- of Pangani = TL ranged 13.5-44.2 cm (n=16); E. coioides
timated using the equation given by Euzen (1987): VI = of Wami = TL ranged 15.3-30.5 cm (n=6); E. coioides of

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(the number of empty stomachs of species i /total number Pangani = TL ranged 15.6-32.0 cm (n=6); P. argenteus of
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of the stomachs of species i examined) × 100. Wami = TL ranged 31.3-41.0 cm (n=5); and S. sihama of
By using the dietary volume data, the standardized Pangani = TL ranged 15.0-25.6 cm (n=8). The extracted
muscle tissues were oven-dried at 60°C and ground to a
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Levin’s (1968) diet niche breadth (Ba) was estimated for
each species in all estuaries following Hurlbert (1978). powder form. A subsample of each sample was weighed to
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The following formula was used: the nearest 0.9 mg and placed into tin capsules for δ13C and
δ15N analysis. The δ13C and δ15N compositions of each sam-
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ple were determined simultaneously using a dual pumped

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Sercon model 20-20 Continuous Flow Isotope Ratio Mass

where Ba is the standardized trophic niche breadth, Pij is Spectrometer (CF/IRMS or EA/IRMS) linked to a Thermo
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the proportion of food category j in the diet of the species model EA1110 Elemental Analyser (EA). The equipment
i and n = total number of food items in the diet of species utilizes dual reaction tubes (combustion/reduction), a mag-
i. The Ba values range between 0, when only one resource nesium perchlorate drier and a Carbosieve G separation col-
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is used, and 1, when all resources are used equally. In ad- umn. Stable isotope results were expressed in the delta
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dition to that, the dietary overlap (O) of the predatory fish notation (δ) relative to the known standards, Vienna Pee
species in each estuary were estimated by using Pianka’s Dee Belemnite (VPDB) for 13C/12C and atmospheric nitro-
index of niche overlap (Pianka, 1973), which considers gen for 15N/14N ratios. The δ13C or δ15N were calculated
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that the different dietary resources are equally accessible using the following formula:
to all species. The formula used was:
δ = [(Rsample/Rstandard) – 1] x 1000

where R is either 13C/12C or 15N/14N.

where Pij and Pik are the proportions of diet category i These isotope analyses were carried out at the OEA
comprised in the diets of j and k, respectively. Both diet Labs Limited in the United Kingdom. Before statistical
niche breadth (Ba) and overlap (O) were considered low analysis of isotopic results, these latter were evaluated to
when the values fall within 0-0.39 range, intermediate gauge if the lipid contents were likely to affect the analy-
when they are within 0.4-0.6, and high when ranged from sis using the C:N ratio (Post et al., 2007). The C:N ratios
0.61-1. of all species were below 3.5, thus, in accordance with
Overall interspecific variations in the diet of the fish Post et al. (2007), the levels of lipids in tissues of fish
species between and within the two estuaries were as- samples were not enough to skew isotopic results. To test
sessed by main and pairwise permutation multivariate the variations in isotopic values among fish species and
analysis of variance (PERMANOVA). The multivariate between estuaries, the isotope data were subjected to main
analysis, including cluster analysis that produces dendro- and pairwise PERMANOVA tests. Two fixed factors,
 Estuarine fish trophic dynamics and anthropogenic disturbances 87

species and estuaries, were considered. The tests were run NND measures the density of species packing, meaning
based on the Euclidian distance resemblance matrix made that species or groups with similar trophic ecologies show
from the normalized isotopic data. smaller values of M-NND and thus represent increased
Furthermore, to enable quantitative comparisons of trophic redundancy. The SD-NND metric indicates the
the trophic niche of fish communities within and between evenness of species packing. This means that lower SD-
the two estuaries, the standard ellipse area corrected for NND is indicative of more even distribution of species, the
small sample size (SEAc), total convex hull area (TA), indictor of higher trophic redundancy as a result of differ-
and other five Layman metrics were estimated using the ent groups having more similar trophic ecologies (Layman
Stable Isotope Bayesian Ellipses in R (SIBER, Jackson et et al., 2007). The SD-NND also show diversification of
al., 2011) package version 4.0.5 (R Core Team, 2021). trophic niches (Donázar-Aramendía et al., 2019).
Standard ellipse area corrected for small sample size and
TA and were estimated as quantitative proxies of the iso-
topic niche width that measure total trophic diversity or RESULTS
niche area. However, these two metrics differ, because
Diet compositions of predatory fish
SEAc is less sensitive to outliers and sample size, as it is
corrected for small sample sizes, than the values of TA. A total of 420 stomachs of four estuarine predatory
For statistical comparison of SEAc between the commu- fish species were examined. Out of that, 332 (79%) con-

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nities investigated, the posterior distribution of the tained food items that were used for further analyses. Ir-

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Bayesian standard ellipse (SEAb) and the 95% credible respective of where species were caught, seven dietary
intervals (CIs) were calculated (Jackson et al., 2011). To items were identified in the stomachs of predatory fish
test whether the isotopic niche space of fish population of species, namely: prey fish, stomatopods, bivalves and

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Wami estuary is larger, smaller or similar to the compa- other unidentified mollusks, prawns, shrimps, polychaetes
rable population of Pangani, the 95% CI of SEAb and TA
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and crabs. Digested materials and remains of hard parts
of those targeted pairs of fish species (see previous para- of preys were also seen in some species. Detrital materials
graphs) were compared. When the CI of distinct pairs of and sand particles were observed as accidental items in-
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species did not completely overlap, the trophic niche of gested by A. africanus. At the species level, the values of
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the comparable populations was significantly different. vacuity index (VI) were considerably high in both estu-
By following Jackson et al. (2011), the probability that aries (Table 1) and the patterns of VI showed that the
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SEAb or TA of species of Wami was smaller than that of predatory fish species were more voracious in Wami rel-
ative to that of the Pangani estuary.
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Pangani was also quantified. The proportions of overlaps

for the comparable groups were also calculated using With the exclusion of polychaetes observed in the
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Bayesian Overlap and compared as they had to match stomachs of both A. africanus and S. sihama, as well as
with the density plot for the 95% prediction ellipsoids. detrital materials found only in the stomachs of A.
The overlaps estimated aimed at describing how much of africanus, all other preys were common in all four preda-
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each species’ niche overlapped with others between and tory fish species under investigation, albeit with different
within the estuaries. volumetric contribution (Table 1). Arius africanus of
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As per Layman et al. (2007), other metrics estimated Wami estuary fed mainly (by volume) on bivalves (27%)
using SIBER package were δ13C range (CR), δ15N range followed by other mollusks (26%) and small fish (19%),
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(NR), mean distance to the centroid (CD), mean nearest while A. africanus of Pangani estuary ingested large
neighbor distance (M-NND) and standard deviation (SD) amounts of bivalves (36%), other mollusks (31%) and
of the M-NND (SD-NND). These Bayesian-derived esti- crabs (9%). Stomatopods and shrimp prey were rarely
mates allow statistical comparisons between communities seen in the stomachs of A. africanus from Wami estuary.
without any restriction on the number of the groups within Fish prey, prawns and crabs were the three most con-
the communities (Layman et al., 2012; Donázar-Ara- sumed preys equally by E. coioides in the Wami estuary,
mendía et al., 2019). The CR was used to indicate trophic whereas prawns, fish, and stomatopods occupied large
diversity or niche diversification at the base of the food percentage of diet for individuals caught in Wami estuary
web. The NR was used to infer both trophic diversity and (Table 1). The diet of P. argenteus of Wami estuary was
the trophic length, meaning that a larger range infers a mainly dominated by prawns and to some extent by fish
wide trophic spectrum. The CD, which is the average Eu- and mollusks, while S. sihama of Pangani estuary ingested
clidian distance of each community component to the cen- large amounts of fish, shrimps, and substantial amounts
troid, was used to infer the average degree of trophic of polychaetes (Table 1). Despite grouping the prey types
diversity. The two metrics, M-NND and SD-NND were at higher taxonomic level, it was noticed that Valamugil
used to evaluate to what extent the trophic redundancy of spp. were dominant among the fish preys encountered in
the fish community vary between the estuaries. The M- the stomachs of all the fish examined.
88 T.J. Lyasenga et al.

Multivariate analyses of dietary composition also revealed that about 50% of the diet of E. coioides of
in predatory fish Wami was shared with P. argenteus from the same estuary
(Figure 2). The prey items consumed by E. coioides popu-
The dendrogram prepared based on the volume of prey lation of Wami were to some extent different (about 40%
items showed that the diet items consumed by the popula- similarity) to that of the population of Pangani estuary. The
tion of A. africanus of Wami and that of the Pangani estu- results further highlighted that the preys consumed by Pan-
aries were highly similar for about 75% (Figure 2). It was gani-drawn E. coioides and S. sihama were far related (40%

Table 1. Diet composition of Arius africanus, Epinephelus coioides, Pomadasys argenteus and Sillago sihama found in their stomachs
and dietary indexes of each prey item: frequency of occurrence (%F), percentage volumetric contribution (%V), number of stomachs
with food/content (n) and vacuity index percentage (%VI).
Food items Wami estuary Pangani estuary
A. africanus E. coioides P. argenteus A. africanus E. coioides S. sihama
(n = 48) (n = 52) (n = 54) (n = 74) (n = 52) (n = 52)
%FO %V %FO %V %FO %V %FO %V %FO %V %FO %V

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Fish 50.0 19.4 51.6 22.4 31.1 11.6 20.8 7.6 64.7 23.2 45.7 33.7
Stomatopods 2.4 1.2 51.6 11.9 13.3 4.0 64.7 19.4 2.9 2.6

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Bivalves 42.9 27.0 9.7 1.5 26.7 9.0 58.3 35.7
Other mollusks 40.5 26.0 26.7 10.1 62.5 31.2 35.3 8.8 22.9 13.1

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Prawns 51.6 22.1 84.4 54.1 16.7 4.8 70.6 32.1
Polychaetes 19.1 5.7 us 20.8 6.5 22.9 17.1
Crabs 35.7 12.0 64.5 22.4 26.7 8.0 31.3 9.3 35.3 12.1 5.7 1.5
Shrimps 14.3 3.6 41.9 14.8 11.8 4.4 28.6 20.6
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Sand/detritus 4.8 3.0 2.1 1.0
Hard tissues/parts 19.4 3.9 2.2 0.9 6.3 1.9
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Unidentifiable/digested 18.1 2.1 6.5 1.0 15.6 2.3 14.6 1.9 25.7 11.4
Vacuity index (VI) 9.76 21.21 15.63 22.58 33.33 23.56
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Figure 2. Dendrogram for hierarchical clustering of dietary composition (by percentage volume) in Arius africanus, Epinephelus
coioides, Pomadasys argenteus and Sillago sihama collected from Pangani (P) and Wami (W) estuaries.
 Estuarine fish trophic dynamics and anthropogenic disturbances 89

average similarity) to each other. The low levels of simi- Variations in stable isotopes of predatory fish
larity in prey consumed by fish were also seen among the and their representative prey fish
E. coioides, A. africanus from the two estuaries and P. ar-
It was revealed that the δ13C and δ15N ratios were sig-
genteus drawn from Wami estuary (40% average similarity,
nificantly different among species and between estuaries
Figure 2). The results of PERMANOVA test paired with
(PERMANOVA, Pseudo-F=27.3, p=0.001; Table 5 and
that of dendrogram showed significant differences among
Figure 4). Moreover, there were significant interactions
species (Pseudo-F=21.0; p=0.001; Table 2) as well as the
interactions between main factors, species, and estuaries
(Pseudo-F=21.0; p=0.001; Table 2). Even the pairwise
PERMANOVA tests indicated spatial intra-specific diet
variations of each of the three pairs of predatory fish species
caught from Wami and Pangani estuaries (t≥1.88; p≤0.05;
Table 3).

Dietary niche breadth and overlaps of predatory species

The values of index of dietary niche breadth (Ba) of

ly
the predatory fish species varied from 0.29 to 0.7 (Figure
3). Despite the dietary volume of E. coioides varied be-

on
tween estuaries (Table 2), the species presented much
higher values of Ba as compared to other species (Figure
3). Arius africanus from Wami showed moderate niche

e
breadth, whereas specimens from Pangani estuary showed us
lower values of Ba (Figure 3). A different situation was
noticed for the comparable pair of P. argenteus from Wami
al
and S. sihama from Pangani where the former species
showed lower, and the latter species showed moderate di-
ci

etary niche breadths (Figure 3). Furthermore, the analysis

er

of dietary overlaps based on Pianka’s index (O) revealed

much high values (O>0.6) for the following pairs: A.
m

africanus of Wami and A. africanus of Pangani, E.

coioides of Wami and E. coioides of Pangani, as well as P.
om

argenteus of Wami and E. coioides of Pangani, (Table 4) Figure 3. Index of dietary niche breadth (Ba) of predatory fish
which is an indication of low trophic flexibility of these species, Arius africanus, Epinephelus coioides, Pomadasys ar-
species in two estuaries. However, the lowest index of genteus and Sillago sihama collected from Wami and Pangani
-c

overlap (O=0.2) was presented by the pair of P. argenteus estuaries. The dotted line indicates the classes of the Ba, 0 – 0.39
on

= low Ba; 0.4 – 0.6 = moderate Ba and 0.61 – 1 = high Ba.

of Wami versus S. Sihama of Pangani (Table 4).
N

Table 2. Two-way PERMANOVA of diet composition in predatory fish species of Arius africanus, Epinephelus coioides, Pomadasys
argenteus and Sillago sihama from Wami and Pangani estuaries. Sq.root CoV = square root component of variation.
Source of variation df MS Pseudo-F p(perm) Sq. root CoV
Estuary 1 10257 4.0 0.002 11.43
Fish species 3 53316 21.0 0.001 33.23
Estuary x Fish species 1 7927.5 3.1 0.012 23.51
Residual 213 2538 50.38

Table 3. Pair-wise PERMANOVA of spatial variations in diet composition of Arius africanus, Epinephelus coioides, Pomadasys ar-
genteus and Sillago sihama from Wami and Pangani estuaries.
Estuary comparisons of fish species Denominator df t p
A. africanus (W) and A. africanus (P) 88 1.88 0.02
E. coioides (W) and E. coioides (P) 46 2.03 0.01
P. argenteus (W) and S. sihama (P) 88 4.17 0.001
90 T.J. Lyasenga et al.

between species and estuaries (PERMANOVA, Pseudo- 13.3±0.3‰) and E. coioides (-18.6±0.7‰; 13.6±0.5‰)
F=22.6, p=0.001; Table 5). At spatial scale, the individual of Wami estuary were significantly lower in terms of δ13C
predatory fish species exhibited a clear distinction of iso- but higher in terms of δ15N ratios when compared to that
topic values between estuaries (Figure 4 and Table 6). As of Pangani estuary (-16.3±2.1; 11.1±1.8‰; -18.0±0.7‰,
such, the mean isotope ratio of A. africanus (-17.3±1.2‰; 12.8±0.6‰ (Figure 4 and Table 6; Pair-wise PER-

Table 4. Niche overlaps between pairs of predatory fish species analyzed from Wami (W) and Pangani (P) estuaries.
Species A. africanus (W) E. coioides (W) P. argenteus (W) A. africanus (P) E. coioides (P) S. sihama (P)
A. africanus (W) 0.42 0.33 0.94 0.42 0.58
E. coioides (W) 0.34 0.25 0.97 0.56
P. argenteus (W) 0.37 0.84 0.21
A. africanus (P) 0.31 0.30
E. coioides (P) 0.49
S. sihama (P)

ly
Table 5. Two-way PERMANOVA results on isotopic variation of predatory fish species at species and estuary level for Arius africanus,

on
Epinephelus coioides, Pomadasys argenteus and Sillago sihama from Wami and Pangani estuaries.
Source df MS Pseudo-F P(perm)

e
Fish species 3 20.85 27.234 0.001
Estuary
Fish species x estuary
1
3
12.43
17.30
16.242
22.606
us 0.001
0.001
Residual 95 0.766
al
ci

Table 6. Pair-wise PERMANOVA results of intraspecific variations in stable isotopes composition of Arius africanus, Epinephelus
coioides, Pomadasys argenteus and Sillago sihama between Wami and Pangani estuaries.
er

Estuary comparisons of fish species Denominator df t p

m

A. africanus (W) and A. africanus (P) 30 4.37 0.001

om

E. coioides (W) and E. coioides (P) 16 2.61 0.004

P. argenteus (W) and S. sihama (P) 23 8.58 0.001
V. buchanani (W) and V. buchanani (P) 26 1.03 0.363
-c
on
N

Figure 4. Bi-plot of mean and standard

error (SE) of carbon and nitrogen stable
isotopes of Arius africanus, Epinephelus
coioides, Pomadasys argenteus and Sillago
sihama and their main prey fish Valamugil
buchanani from Wami and Pangani river
estuaries.
 Estuarine fish trophic dynamics and anthropogenic disturbances 91

MANOVA, t=4.4, p≤0.004). Similarly, the stable isotope for other metrics of trophic niche width of A. africaus,
ratio of S. sihama based in Wami when compared with P. such as the Bayesian estimate of trophic niche width
argenteus of Pangani, were significantly variable. This (SEAb) and SEAc (Figure 5 and Table 7). Likewise, the
meant that the isotopic ratios of S. sihama of Pangani es- same trend was also noticed for the SEAb and SEAc of
tuary exhibited the lowest δ13C (-20.1±1.7‰) and higher the other three pairs of species of comparison from Wami
δ15N (12.8±0.5‰) values when compared to that of P. ar- and Pangani estuaries (Figure 5 and Table 7). The results
genteus from Wami estuary (-15.5±0.2‰, 12.4±0.1‰; of the intra- and interspecific comparisons of SEAb within
Figure 4). For the potential prey-fish, V. buchanani despite and between the estuaries varied from one pair to another
the δ13C and δ15N mean values being slightly higher in of predatory species. The SEAb of A. africanus from
Wami compared to that of Pangani (Figure 4), the isotopic Wami was significantly smaller than that of Pangani es-
variations were statistically not significant (pairwise PER- tuary with no intraspecific overlap in between Bayesian
MANOVA, t=1.03, p>0.05; Table 6). estimate of 95% CI (Table 7). This was also in line with
estimate of the probability of SEAb of less than 1% for
Isotopic trophic diversity, niche width and overlaps the A. africanus based in Pangani to be smaller than that
of fish populations of Wami estuary (Table 7). The SEAb of E. coioides from
both Wami and Pangani estuaries were statistically similar
The CR (that measures the trophic diversity) and NR to each other due to large overlaps between 95% CI and

ly
(measuring trophic length and diversity) of A. africanus 50% in magnitude of probability of the SEAb for the two
were shorter in the Wami estuary compared to that of the

on
pairing species (Table 7). Even CR and NR of E. coioides
Pangani estuary (Table 7). The situation was also similar

e
us
Table 7. Bayesian standard ellipse area widths (SEAb), magnitude of probability of SEAb for the Wami-based species to be smaller
than Pangani based estuarine species; SEAc, CR and NR for A. africanus, E. coioides, S. sihama, P. argenteus and V. buchanani studied
in Wami and Pangani estuaries. CI – credible interval of 95%.
al
Species Wami Pangani Probability (%)
ci

of SEAb
for species
er

of Wami < Pangani

for 95%CI
m

%CI Lower Upper %CI Lower Upper

om

A. africanus 99 0.59 2.31 99 1.99 8.04

95 0.68 1.92 95 2.36 6.67 0.0005
50 0.95 1.35 50 3.20 4.60
-c

Mode 1.11 3.81

SEAc 1.26 3.69
CR 3.56 7.00
on

NR 0.92 3.44
E. coioides 99 0.37 3.09 99 0.44 2.86
N

95 0.47 2.27 95 0.56 2.20

50 0.78 1.29 50 0.89 1.38
Mode 1.00 1.09
SEAc 1.27 1.32
CR 1.86 1.51
NR 1.50 1.46
P. argenteus (Wami)/S. sihama (Pangani) 99 0.02 0.11 99 0.84 4.03
95 0.02 0.09 95 0.99 3.20
50 0.04 0.05 50 1.49 2.18 50
Mode 0.04 1.81
SEAc 0.05 1.98
CR 0.61 4.38
NR 0.26 1.52
V. buchanani 99 0.87 4.36 99 1.34 5.89
95 1.06 3.53 95 1.67 4.77
50 1.57 2.35 50 2.39 3.37 -
Mode 1.91 2.85
SEAc 2.18 3.19
CR 2.4 2.98
NR 2.55 2.56
92 T.J. Lyasenga et al.

from these estuaries were relatively similar. The SEAb, vealed that SEAb of Wami was slightly smaller than that
and thus, trophic niche width, of S. sihama of Pangani was of Pangani as they showed substantial overlap between
significantly larger as compared to that of A. argenteus of the 95% CI (Wami estuary 3.90-6.94 of 95% CI; Pangani
Wami due to zero overlap between the 95% CI (Table 7). estuary 5.70-9.69 of 95% CI). However, the magnitude of
Contrary to that, the substantial overlap between the 95% probability for SEAb of Pangani to be smaller than that
CI for the V. buchanani from both Wami and Pangani es- of Wami was impossible to occur (<1%). More so, the
tuary (Table 7) was considered as an indication that the high level of overlap between SEAc of two estuaries was
trophic niche width of the species in these habitats is
noticed whereby the SEAc of Wami was greatly enclosed
somewhat similar. Furthermore, the SEAb between the
within that of Pangani estuary (Figure 6).
following pairs of species were also significantly different
As well, the Layman community indices showed that
when their 95% CIs were compared: both pairs of A.
Africanus versus E. coioides from within Pangani and the two estuaries differ in trophic resources and level of
Wami estuaries, E. coioides versus P. argenteus of Wami trophic diversifications of the same fish species investi-
as well as A. Africanus versus P. argenteus of Wami estu- gated (Figure 7). The trophic length as indicated by the
ary (Table 7). Similar to A. africanus, the CR and NR of NR of Pangani estuary (NR=2.45) was marginally shorter
S. sihama (CR=4.4‰, NR=1.5‰) and V. buchanani when correlated with that of Wami (NR=2.91; Figure 7).
(CR=3.0‰, NR=2.6‰) were consistently higher in Pan- The opposite situation was noticed for the indicator of

ly
gani estuary than those of their comparable species in the

on
Wami estuary (P. argenteus CR=0.6‰, NR=0.3‰; and V.
buchanani CR=2.4‰, NR=2.5‰; Figure 5 and Table 7).
The SEAc showed substantial overlap between the

e
standard ellipses for A. africanus and E. coioides from
Wami estuary, and between all comparable species from
Pangani estuary (Figure 5). This indicated that the degree
us
of dietary resource sharing by predatory fish was higher
al
in Pangani compared to that of Wami estuaries. Specifi-
cally, the estimates of SEAc overlap analyses revealed
ci

that, in Wami estuary, the percentage of overlap between

er

SEAc for A. africanus onto that of E, coioides, and vice

versa, was 54%. No overlap of SEAc was found between
m

A. africanus versus P. argenteus nor E. coioides versus P.

om

argenteus from Wami estuary. Contrary to that, in Pangani

estuary, the largest percentages of overlap were indicated
by SEAc for the S. sihama onto that of A. africanus (62%)
-c

and for the E. coioides onto that of A. africanus (61%).

The percentage of SEAc for the A. africanus versus E.
on

coiodes was 21% and A. africanus versus S. sihama was

34%. More so, the percentage of E. coioides that over-
N

lapped with S. sihama was 58%, while that of S. sihama

onto the SEAc of E. coioides was 16%. The results of
intra-specific overlap between estuaries indicated that the
SEAc for the A. africanus of Pangani onto that of Wami
was 11%, but the values of the overlap for the vice versa
was 33%. For the E. coioides, the overlap percentages be-
tween estuaries were 57% and 59%. Again, there was no
ellipse overlap for the P. argenteus of Wami and S. sihama
of Pangani.
Figure 5. The convex hull area (dotted lines) and standard el-
Trophic niche and redundancy at estuary level lipse areas (SEA) measuring the trophic niche width of individ-
ual predatory fish: 1.1 Arius africanus from Pangani; 2.5 A.
The SEAc and TA that infer the total trophic niche area africanus of Wami; 1.2 Epinephelus coioides of Pangani; 2.6 E.
of fish community were smaller in Wami (SEAc=5.4; coioides of Wami; 1.3 Sillago sihama of Pangani; 2.7 Po-
TA=14.6) contrary to that of Pangani estuaries madasys argenteus of Wami and their prey fish; 1.4 = Valamugil
(SEAc=7.6; TA=25.1; Figure 6). The comparison test for buchanani from Pangani and 2.8 = V. buchanani of Wami and
the Bayesian estimate 95% CI of the two estuaries re- Pangani estuaries.
 Estuarine fish trophic dynamics and anthropogenic disturbances 93

basal and average trophic diversity of fish as expressed

by the CR and CD (Figure 7). The trophic redundancy
(measured as M-NND) and its standard deviation
(SDNND) differed substantially between the two estuaries
with M-NND being smaller and SDNND larger in Wami
than Pangani estuary (Figure 7).

DISCUSSION
The findings of this study indicate how anthropogenic
activities in the upstream of the river catchments induce
changes to the estuarine ecosystem’s functioning. The re-
Figure 6. Trophic niche width indicated by TA (dotted lines) sults suggest that despite the Wami estuary being under
and SEA (solid lines) for the pooled stable isotopes of carbon conservation status, the high level of disturbances up-
and nitrogen of fish from Wami and Pangani estuaries (n = 103).
stream of the river increase vulnerability of the estuarine
Cycle points represent individuals of all the species measured
in each estuary and standard ellipse/circle represent the maxi- food web structure and ecosystems functioning. This is
probably connected to a lower primary production, to

ly
mum likelihood of isotopic niche of the species analyzed.
changes in trophic positions of consumers, and thus to

on
modifications occurring in the trophic niche of the preda-
tory fish. As a result, the reduced trophic diversity, eco-
logical redundancy, and complexity of the ecosystem are

e
most likely experienced in Wami estuary than Pangani es-
us
tuary. This was different from the expectation as the con-
sidered highly disturbed Pangani estuary presented a
relatively stable, resilient, and ecologically redundant
al

ecosystem.
ci

Even though our findings are based on few compo-

nents of the estuarine food webs, they include important
er

compartments that greatly shape the complexity and thus

m

determine the ecological redundancy of the estuarine

ecosystems of concern. Furthermore, the inferences drawn
om

from the present study are based on data collected in a spe-

cific seasonal period, so that isotopic values gathered from
estuarine fish with large body size (i.e., predatory fish)
-c

mirror the exploitation of natural resources during their

on

growth period. Moreover, data collection that adheres to

seasons may elucidate more on long-term changes in the
use of dietary resources and other niche characteristics of
N

estuarine fish assemblage. Moreover, our results explain

how both predatory and prey fish respond to the dynamics
of dietary resources, representing with a good approxima-
tion the food web state in tropical estuaries differing in the
degree of anthropogenic disturbances.
Our findings showed that both stomach contents and
Figure 7. The estuarine community-wide Layman metrics of stable isotopes can reveal significant differences in diet
Wami and Pangani estuaries that showed the (i) trophic length,
and isotopic values among fish species in different estu-
or complexity, NR (dY_range), (ii) trophic diversity, or CR
(dX_range), (iii) niche width, or convex hull area (TA), (iv) av- aries. Matching of these findings confirm that both meth-
erage trophic diversity, or mean distance to the centroid (CD), ods can characterize the foraging flexibility of predatory
(v) trophic redundancy, or the mean nearest neighbor distance fish species of marine origin in estuaries. Except for A.
(NND), and (vi) evenness of species packing, or extent of africanus, the results of the index of dietary niche breadth,
trophic diversification, that is, the standard deviation ) of NDD Ba, have matched well with that of isotopic trophic niche
(SDNND). Black dots are the modes, boxes indicate the credible metrics of the species between estuaries. As such, the ob-
intervals at 50%, 75% and 95%. The numbers above each box served consistent highest Ba of E. coioides in both estu-
are modes; the cross (red) is the values of the true population. aries correlated with the similarity in their SEAb between
94 T.J. Lyasenga et al.

estuaries. Similarly, the estimated moderate Ba of S. si- environmental change. This is further indicated by the dis-
hama from Pangani and the lowest Ba of P. argenteus similarity in magnitude of the isotopic metric-based over-
from Wami correlated with the larger SEAb of Pangani- lap of each possible pair of the predatory fish species in
based S. sihama versus the comparable smaller SEAb of the two estuaries examined. The highest degree of overlap
P. argenteus of Wami estuary. However, the mismatch of for the fish species of Pangani might be an indication of
trophic feeding niche of A. africanus by the two methods shifts in the trophic positions of organisms preyed upon
indicates that the trophic dynamics in highly fluctuating by these species in two estuaries resulting to the observed
estuarine ecosystems requires robust methods that should differences in trophic length, diversity and trophic niches
complement the conventional stomach content analysis justified by NR, CR, CD and SEAc/SEAb. The shifts in
for drawing a sound and logical conclusion. The applica- trophic positions of consumers within comparable aquatic
tion of stable isotope in trophic ecology studies is widely environment is mainly driven by differences in individual
accepted (e.g. Pasquaud et al., 2010; Olsen et al., 2011; diet, trophic discrimination or enrichment factor (Villa-
Layman et al., 2012; Cummings et al., 2012) as it is marín et al., 2018), as well as differences in the level of
among the powerful tools that ensure the determination nutrients load fueling the base of the food web (Warry et
of the integrated diet consumed and assimilated at a al., 2016).
coarse taxonomic scale but over a long period (Michener Furthermore, our findings suggest a possibility of
and Lajtha, 2007; Selleslagh et al., 2015). Relative to that, presence of ontogenetic shift in trophic positions (Park et

ly
the stomach content analysis determines the diet ingested al., 2018; Villamarín et al., 2018) for the comparable es-

on
instantly by the consumers at a finer taxonomic level (Ma- tuaries examined herein. Although the length size of the
hesh et al., 2018). individuals was not considered during analysis, it might
The marked variations in the dietary composition and also influence the results of the differences in isotopic val-

e
trophic niche among the predatory fish species found in ues of the species between the estuaries. This is mainly
our study imply that they largely consume similar preys
us
linked with the size range (total length, TL) of A.
but in different proportions in the two estuaries. Differ- africanus from Wami versus of Pangani and P. argenteus
ences in the amounts of preys consumed may be linked of Wami versus S. sihama of Pangani. The literatures em-
al

to the prey abundance and catchability along with prey phasize that resource utilization patterns of fish change
ci

visibility by predatory species, plus the feeding strategies markedly with ontogeny (Davis et al., 2012; Park et al.,
and energy requirements (Kulbicki et al., 2005; Kroetz et 2018; Villamarín et al., 2018).
er

al., 2016). Both stomach contents and stable isotope-de- Specifically, with the exclusion of E. coioides, the
m

rived Layman metrics showed a considerable degree of larger CR of predatory fish populations of Pangani estuary
trophic resource sharing and thus trophic niche overlaps might be linked with their prey to feed on the diet with
om

among these predatory fish in estuaries. This finding varied nutritional sources. The largest SEAb of A.
agrees with those from the study of Matich et al. (2017). africanus population of Pangani could be probably asso-
This possibly does not imply competition in trophic re- ciated with a high level of opportunistic or generalist feed-
-c

sources but rather the prey-catch strategies that define the ing mechanism as a coping strategy resulting from
prey types consumed. For instance, the higher trophic exposing the estuary to more frequent human perturba-
on

niche breadth and similarity in isotopic niche width of E. tions. The smallest SEAb of P. Argenteus of Wami and its
coioides in Wami and Pangani estuaries could be favored δ13C mean values (-15.5±0.2‰) is an indication that the
N

by its ambush strategy and structural complexity of the riverine or terrestrial derived dietary sources of which
estuaries (Gibran, 2007). Complex habitats such as these their δ13C ratio range from -23 to -30‰ (Bouillon et al.,
mangrove-sheltered estuaries provide enhanced cover that 2011) had little influence on the diet dynamics of this
reduces the possibilities of predators to be detected by the species. This is somewhat contributed by the sampling lo-
preys (Mwijage et al., 2018a). This situation is probably cation of the samples. Pomadasys argenteus was caught
connected with the highest overlap of SEAc of the species in the estuarine plume away from the river mouth, and
between estuaries. this environment might have been less influenced by the
Inter- and intra-species variations in isotopic values riverine dietary sources. The same situation further ex-
could mean considerable individual variability in the feed- plains the observed non-overlap of SEAc between P. Ar-
ing strategies with individuals consuming prey of different genteus and any other pair of predatory fish studied. More
trophic spectra and the use of basal nutritional sources so, the similarity in SEAb of E. coioides between estuaries
they rely on. Differences in both dietary niche breadth and suggests low trophic niche flexibility of the species. In
isotopic niche width at the estuary level suggest that fish view of that situation, the environmental filtering hypoth-
species may have high trophic niche plasticity or flexibil- esis plays a role in this assembly that was not similar due
ity, which is indicated by Matich et al. (2017) as a mech- to divergence in the environmental conditions of the
anism to respond to natural and human-induced species habitats (Pereira et al., 2017).
 Estuarine fish trophic dynamics and anthropogenic disturbances 95

Furthermore, the higher values of δ15N and NR of and hence small SEAc of fish populations and communi-
Wami-associated species may be an indication of the ties in the Betsiboka and Tana estuaries.
predatory fish to occupy higher trophic position usually The predatory fish assemblages in the Wami estuary
connected to the nature of the diet assimilated by individ- are probably less opportunistic in feeding that implies a
uals, the trophic enrichment factor and high levels of nu- low level of resilience upon disturbances. Selleslagh and
trients load (Villamarín et al., 2018), as opposed to Amara (2014) also showed that fish in the Canche Estuary
Pangani estuary. The effects of high values of δ15N at low showing very low anthropogenic pressure, exhibited a
trophic level are transmitted upwards higher up to top specialist feeding strategy. The resilience of the estuarine
predators of estuarine food web, thus affecting the overall ecosystem is contributed by among others, trophic com-
trophic organization (Warry et al., 2016). Parallel to this, plexity or multiplicity of trophic linkages along the
the substantial low δ13C ratio could be contributed by the trophic web and species diversity (Lira et al., 2018). In
Wami estuarine food web to be fed by riverine primary that sense, the present study agreed with the findings of
food sources and high inorganic nitrogen load that elevate Pasquaud et al. (2010) and Donázar-Aramendía et al.
δ15N values in secondary production (Michener and La- (2019) who showed that high degrees of anthropogenic
jtha, 2007; Woodland and Secor, 2011; Warry et al., pressures modify the structural components and ecologi-
2016). In the Pangani estuary, water abstractions upstream cal roles of the species in estuarine ecosystems.
of the river due to multi-reservoirs for hydropower gen- Structural modifications in Wami estuary are certainly

ly
eration and irrigation is linked with trophic interactions influenced by the high turbidity that, apart from affecting

on
downstream the estuarine and coastal food webs (Mwi- primary production, hampers species of higher-order con-
jage et al., 2018b). These human activities contributed to sumers or predatory fish because of lower performances
modify the nutrients’ biogeochemistry in the estuary and in prey hunting. The reduction of predatory fish species

e
increased retention time of sediment, organic particles and from a community lead to the dominance of its prey at the
accompanied nutrients in the reservoirs, upstream of Pan-
us
lower trophic level and subsequent secondary extinctions
of other carnivores (Sanders et al., 2018). This also leads
gani river (Selemani et al., 2017). Eventually, Pangani es-
tuary experience lower δ13C values of terrestrial derived to a reduction in trophic redundancy and consequently
al

basal food sources (Mwijage et al., 2018a) and regulated complexity and stability of the estuarine food webs. On
the other hand, the large degree of overlaps in the isotopic
ci

nutrients load including nitrogen compounds.

At the estuarine level, the differences in mean distance niche of species from the Pangani estuary could not imply
er

to the centroid (CD) and SEAc of the Wami and Pangani the existence of potential competitions of the trophic re-
sources but rather the similarity in environmental condi-
m

fish species may be linked to the variations in estuarine

primary productivity. The high loads of suspended sedi- tions in microhabitats the fish species used for feeding.
om

ments in the Wami estuary as reported by Kiwango et al. Greater diet overlaps increase trophic redundancy of the
(2015) contribute to reducing trophic diversity and abun- ecosystem (Sanders et al., 2018), a contention that seems
dance resulting from the low rate of aquatic primary pro- to agree with our results which show that the Pangani es-
-c

duction (Selemani et al., 2017). Light penetration is tuary has greater trophic redundancy than that of Wami.
constrained by the suspended particles that, consequently,
on

limit photosynthetic activities. In that way, trophic web

connectance, or the number of trophic links to the primary CONCLUSIONS
N

producers, tend to be small. This also may be a factor con- Overall, the community-wide metrics derived from sta-
tributing to the low level of trophic overlap of Wami and ble isotopes when complemented with dietary data eluci-
consequently, low trophic redundancy (de Carvalho et al., date how predatory fish and their prey respond to
2017; Lira et al., 2018). The overall effect is to make food human-induced changes in trophic niche width; this re-
web components vulnerable to secondary extinctions as a sponse determines cascading effects that impact the trophic
result of the reduced complexity of the ecosystem (Lira redundancy and complexity of the estuarine ecosystems.
et al., 2018). This supports our findings but not what was Our findings indicate that anthropogenic activities in the
expected of Wami to exhibit higher trophic redundancy upstream modified higher trophic position of fish con-
than Pangani. As such, Wami estuary presented a large sumers in Wami relative to that of Pangani estuaries. Thus,
SD-NND which suggests a reduced trophic redundancy. without management interventions, food web structure re-
This is in contrast to the Pangani estuary that according organization and disruption are likely to occur within the
to Hellar-Kihampa et al. (2013), have relatively low sed- above-mentioned estuaries. Moreover, our findings should
iment loads as large volumes are retained in the dams lo- be taken with the caveat that not all components of the es-
cated upstream of the estuary. This concurred with the tuarine food webs were used to draw such inferences, but
findings of Abrantes et al. (2014) who reported that the they could be used as indicators of showing that the two
high sediment loads affect aquatic primary productivity estuarine systems investigated are ecologically disturbed
96 T.J. Lyasenga et al.

by anthropogenic activities. Therefore, management initia- portance of terrestrial subsidies for estuarine food webs in
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Anderson EP, McNally C, Kalangahe B, Gutmann Roberts C,
Corresponding author: Alistidia Paul Mwijage, Tanzania Fisheries
Research Institute (TAFIRI) – Headquarters, P. O. Box 9750, Dar Britton JR, 2018. Quantifying trophic interactions and niche
es Salaam, Tanzania. sizes of juvenile fishes in an invaded riverine cyprinid fish
E-mail: alistidiamwijage@tafiri.go.tz; zawadi2007@gmail.com. community. Ecol. Freshw. Fish 27:976-987.
Anderson EP, McNally C, Kalangahe B, Ramadhani H, Mhitu
Key words: diet; predatory fish; stable isotope; trophic niche; Lay- H, 2007. A rapid ecological assessment of the Wami river
man community metrics; anthropogenic disturbances estuary, Tanzania. Available at: https://pdf.usaid.gov/pdf_
docs/pnadn793.pdf : 38 pp.
Funding: The University of Dar es Salaam through the CoAF-
AQF19058 project number covered all costs from the study design
Baeta A, Valiela I, Rossi F, Pinto R, Richard P, Niquil N, et al.,
through data collection and interpretation of results. 2009. Eutrophication and trophic structure in response to the
presence of the eelgrass Zostera noltii. Mar. Biol. 156:2107-
Acknowledgements: The authors acknowledge the funder of this 2120.
study, the University of Dar es Salaam that covered all costs from Beck MW, Heck KL, Able KW, Childers DL, Eggleston DB,
the study design through data collection and interpretation of the 2001. The identification, conservation and management of

ly
results. The authors also recognize and appreciate the technical estuarine and marine nurseries for fish and invertebrates.

on
support and research facilities provided by the Chemistry depart-
Bioscience 51:633-641.
ment of the College of Natural and Applied Sciences and School
of Aquatic Sciences and Fisheries Technology of the University of Bianchi G, 1995. FAO species identification sheets for fishery
Dar es Salaam. The support of Dr. Blandinga Lugendo (from Uni- purposes. Field guide to the commercial marine and brack-

e
versity of Dar es Salaam) who assisted the logistics of identifica- ish-water species of Tanzania. Prepared and published with
tion of a laboratory in United Kingdom to undertake the stable
isotope analysis is also appreciated. The authors also acknowledge
us the support of TCP/URT/4406 and FAO (FIRM) Regular
Programme. Rome, Italy.
and appreciate the technical support and research facilities pro- Bouillon S, Connolly RM, and Gillikin DP, 2011. Use of stable
vided OEA Labs limited in the United Kingdom.
al
isotopes to understand food webs and ecosystem functioning
Authors’ contributions: All authors played different roles through- in estuaries. In: Wolanski E, McLusky DS (eds.), Treatise
ci

out the production of this manuscript. Project conceptualization on estuarine and coastal science, 7:143-173.
Carbonara P, Follesa MC, (eds.) 2019. Handbook on fish age
er

was conducted by TJL, DAS, JAMM and LG. Data curation was
conducted by PLM and DAS. Methodology and formal data analy- determination: a Mediterranean experience. Studies and Re-
sis were conducted by PLM, APM, TJL and DAS. Manuscript writ- views. FAO. No. 98. Rome, Italy : 192 pp.
m

ing (original draft) was done by APM, TJL, DAS and PJM. Cole ML, Kroeger KD, Mcclelland JW, 2016. Effects of water-
Visualization and the first draft manuscript review were performed
om

shed land use on nitrogen concentrations and δ15 Nitrogen in

by DAS, JAMM, LG and DAS. Funding was collectively solicited
by PLM, DAS, JAMM, LG and DAS.
groundwater. Biogeochemistry. 77:199-215.
Cummings DO, Buhl J, Lee RW, Simpson SJ, Holmes SP, 2012.
Estimating niche width using stable isotopes in the face of
-c

Conflict of interest: The authors declare no potential conflict of in-

terest. habitat variability: a modelling case study in the marine en-
on

vironment. PLoS ONE. 7:e40539.

Availability of data and materials: All data generated or analyzed Davis AM, Blanchette ML, Pusey BJ, Jardine TD, Pearson RG,
during this study are included in this published article. 2012. Gut content and stable isotope analyses provide com-
N

plementary understanding of ontogenetic dietary shifts and

Received: 18 July 2021.
Accepted: 24 November 2021. trophic relationships among fishes in a tropical river.
Freshw. Biol. 57:2156-2172.
This work is licensed under a Creative Commons Attribution Non- de Carvalho DR, de Castro DMP, Callisto M, Moreira MZ, Pom-
Commercial 4.0 License (CC BY-NC 4.0). peu PS, 2017. The trophic structure of fish communities
from streams in the Brazilian Cerrado under different land
©
Copyright: the Author(s), 2021 uses: an approach using stable isotopes. Hydrobiologia
Licensee PAGEPress, Italy
795:199-217.
Advances in Oceanography and Limnology, 2021; 12:9987
DOI: 10.4081/aiol.2021.9987
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gurgitation in the grouper Cephalopholis argus. J. of Appl.
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