Edited by: John Pascal Simaika, IHE Delft Institute for Water Education, Netherlands
Reviewed by: Martin Paar, University of Greifswald, Germany; Guillaume Grosbois, Université du Québec à Chicoutimi, Canada
This article was submitted to Freshwater Science, a section of the journal Frontiers in Environmental Science
†ORCID: Jaclyn M. Hill
Olaf L. F. Weyl
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In Africa, wetlands, such as shallow, ephemeral lakes provide ecosystem services, such as water purification, food supply, and flood control but are subject to dynamic flooding/drying cycles which vary in duration from years to decades. The stochastic nature of drying events subjects ephemeral lake fauna to persistent disturbance regimes, therefore understanding how biota respond to flooding and drying events is essential for their conservation and management. Primary production sources supporting consumer biomass in the shallow ephemeral Lake Liambezi (upper Zambezi Ecoregion), were investigated using stable isotope analysis, mixing models and stomach content analysis to investigate the following hypotheses: (1) algal primary production supports a higher consumer biomass than aquatic macrophytes; (2) the lake food chain is short, because the majority of fish fauna are detritivorous/herbivorous cichlids that are consumed by top predators; (3) fish community trophic structure will be similar between years; and (4) with short food chains and stochastic resource availability, there will be substantial competition for food among fish species. Results showed that phytoplankton production supported substantial consumer biomass in Lake Liambezi, with important contributions from macrophytes and associated detritus and/or periphyton. While particulate organic matter (POM) contributed substantially to the diet of herbivorous/detritivorous tilapiine cichlids (the backbone of Lake Liambezi's commercial fishery), considerable dietary carbon was likely also derived from aquatic plants and associated detritus and/or periphyton compared to other fishes. Three major food chains were identified in the lake. The phytoplankton-based pelagic food chain was longest, involving up to four trophic transfers. The benthic food chain based primarily on detritus of planktonic origin (but may also include macrophyte associated detritus/periphyton) was characterized by high levels of omnivory and involved up to three trophic transfers. The macrophytic detritus-based food chain was shortest, involving just two trophic transfers. Predators fed across all three food chains, but predominantly on the two benthic food chains. A combination of dietary overlap (amongst piscivores/predators, amongst insectivores), dietary specialization (tilapiine cichlids, alestids), the integration of multiple food chains and behavioral adaptation to changing dietary resources underpins the ability of Lake Liambezi's fish community to thrive under the stochastic nature of ephemeral lake ecosystems.
Wetlands are diverse and productive systems (Ward et al.,
Seasonal variation in the hydrological regime of tropical lakes becomes more pronounced with increasing latitude (Talling,
Lake Liambezi is a shallow ephemeral floodplain lake situated in north-eastern Namibia. It is fed on an irregular basis by the Upper Zambezi and Kwando rivers, which overflow into the lake during years of extremely high flooding (Peel et al.,
This paper aims to investigate which primary production sources support consumer biomass in Lake Liambezi, a shallow ephemeral lake located in the upper Zambezi Ecoregion, to describe the trophic structure of the fish community and assess the trophic interactions among fish species, in order to discuss their potential influences in shaping its fish community. Using stable isotope analysis, mixing models and complimentary stomach contents analysis (fish only), this study set out to investigate the following hypotheses: (1) algal primary production (phytoplankton) supports a higher proportion of consumer biomass than aquatic macrophytes; (2) the lake food chain will be short, as a large component of the fish fauna comprises detritivorous and herbivorous fishes that may be consumed directly by top predators; (3) fish community trophic structure will be similar between years; and (4) with short food chains and the stochastic nature of resource availability in ephemeral systems, there will be substantial competition for food resources among fish species.
Lake Liambezi is a shallow ephemeral floodplain lake situated in the Zambezi Region of Namibia in southern Africa (
Map of north-eastern Namibia illustrating the rivers and floodplains feeding into Lake Liambezi, and the location of the Lake Liambezi sampling site.
Stable isotope samples were collected during August 2011 and August 2012. Limited sampling of basal resources and fishes [
All samples were oven dried at 50°C for 24–48 h, ground to a homogenous powder and then analyzed for δ13C and δ15N using a Europa Scientific 20-20 IRMS linked to an ANCA SL Prep Unit at IsoEnvironmental cc, South African Institute for Aquatic Biodiversity, Grahamstown, South Africa. Isotope values are expressed in delta notation according to:
where
Ethics approval was granted by the SAIAB Animal Ethics Committee (2013-07).
All fish samples were lipid corrected as described by Taylor et al. (
To investigate the proportional contribution of resources underpinning Lake Liambezi food webs separately for each year, Bayesian mixing models (MixSIAR; Stock and Semmens,
Carbon and nitrogen stable isotope values (mean ± standard deviation) of fish species, invertebrate groups and basal carbon sources sampled in Lake Liambezi in 2011 and 2012, and the taxonomic/feeding group to which species were assigned for broad food web analysis.
Alestidae | 28 |
−26.71 ± 1.40 | 9.82 ± 0.85 | 32 |
−27.89 ± 2.20 | 9.81 ± 0.98 | Alestids | |
Alestidae | 21 |
−27.97 ± 0.93 | 9.89 ± 0.41 | 10 |
−26.15 ± 1.31 | 9.64 ± 0.62 | Alestids | |
Cyprinidae | 1 | −29.16 | 8.71 | – | – | – | Cyprinids | |
Cyprinidae | 3 | −21.66 ± 1.19 | 7.36 ± 0.37 | 7 | −31.31 ± 0.99 | 9.11 ± 0.88 | Cyprinids | |
Cyprinidae | 6 | −24.45 ± 0.84 | 8.26 ± 0.39 | – | – | – | Cyprinids | |
Cyprinidae | 8 | −23.14 ± 2.96 | 8.25 ± 0.81 | 2 | −27.10 ± 0.70 | 8.36 ± 0.03 | Cyprinids | |
Cyprinidae | 21 |
−25.55 ± 2.01 | 8.38 ± 0.56 | 11 |
−26.32 ± 0.46 | 8.50 ± 0.89 | Cyprinids | |
Cyprinidae | 9 | −27.07 ± 0.80 | 9.04 ± 0.36 | – | – | – | Cyprinids | |
Cyprinidae | 3 | −26.85 ± 2.21 | 9.90 ± 0.55 | – | – | – | Cyprinids | |
Cyprinidae | 1 | −24.27 | 7.78 | 1 | −24.54 | 8.03 | Cyprinids | |
Cichlidae | 21 |
−26.94 ± 2.02 | 8.46 ± 0.76 | 16 |
−27.60 ± 2.28 | 8.92 ± 1.17 | Benthic cichlids | |
Cichlidae | 17 |
−24.00 ± 2.41 | 9.42 ± 0.73 | 5 | −23.89 ± 1.05 | 8.54 ± 0.79 | Benthic cichlids | |
Cichlidae | 20 |
−24.68 ± 2.12 | 8.30 ± 0.69 | 1 | −23.93 | 8.82 | Benthic cichlids | |
Cichlidae | – | – | – | 3 | −25.37 ± 2.62 | 9.47 ± 1.66 | Benthic cichlids | |
Schilbeidae | 25 | −25.26 ± 2.24 | 8.95 ± 1.04 | 29 | −26.08 ± 1.82 | 9.50 ± 0.83 | Generalist predators | |
Clariidae | 11 | −24.46 ± 2.20 | 8.92 ± 0.46 | 1 | −24.23 | 9.8 | Generalist predators | |
Clariidae | 1 | −22.93 | 10.55 | – | – | – | Generalist predators | |
Mochokidae | 17 | −27.84 ± 2.01 | 9.25 ± 0.88 | 3 | −26.81 ± 0.36 | 10.30 ± 0.51 | Generalist predators | |
Mormyridae | 13 |
−25.67 ± 2.27 | 7.51 ± 0.76 | 2 | −27.74 ± 3.52 | 7.70 ± 0.21 | Mormyrids | |
Mormyridae | 7 | −26.08 ± 1.01 | 9.11 ± 0.55 | 6 | −25.59 ± 1.74 | 8.93 ± 0.40 | Mormyrids | |
Mormyridae | 1 | −30.63 | 9.3 | – | – | – | Mormyrids | |
Mormyridae | – | – | – | 1 | −26 | 9.2 | Mormyrids | |
Cichlidae | 16 | −25.49 ± 2.21 | 10.35 ± 0.78 | 10 | −25.56 ± 2.12 | 10.48 ± 1.33 | Piscivores | |
Cichlidae | 3 | −20.57 ± 0.65 | 9.37 ± 0.41 | 1 | −21.59 | 9.37 | Piscivores | |
Hepsetidae | 11 | −23.69 ± 1.99 | 9.91 ± 0.80 | 10 | −24.61 ± 3.19 | 10.36 ± 1.32 | Piscivores | |
Clariidae | 5 | −24.74 ± 2.36 | 9.88 ± 0.46 | 7 | 24.33 ± 1.62 | 10.04 ± 0.73 | Piscivores | |
Cichlidae | 10 |
−26.14 ± 4.09 | 6.34 ± 0.88 | 20 |
−27.90 ± 1.97 | 7.73 ± 1.41 | Tilapiine cichlids | |
Cichlidae | 12 |
−22.46 ± 1.89 | 5.38 ± 0.68 | 14 |
−24.49 ± 2.76 | 5.15 ± 0.90 | Tilapiine cichlids | |
Cichlidae | 18 |
−21.92 ± 3.86 | 7.12 ± 0.98 | 10 |
−25.75 ± 2.47 | 6.70 ± 1.14 | Tilapiine cichlids | |
Cichlidae | 16 |
−24.55 ± 1.78 | 7.60 ± 1.38 | 18 |
−26.95 ± 3.44 | 7.54 ± 1.35 | Tilapiine cichlids | |
Cichlidae | 2 | −21.74 ± 1.08 | 8.18 ± 1.17 | – | – | – | Tilapiine cichlids | |
Poeciliidae | 11 |
−26.20 ± 2.11 | 9.78 ± 0.50 | 6 | −23.92 ± 1.00 | 8.34 ± 0.53 | Topminnows | |
Poeciliidae | – | – | – | 4 | −22.06 ± 0.72 | 8.31 ± 0.38 | Topminnows | |
Aquatic insects | – | 10 | −28.32 ± 3.62 | 6.14 ± 2.79 | 24 | −26.67 ± 2.40 | 5.95 ± 1.30 | – |
Decapods | – | 10 | −23.96 ± 0.94 | 7.22 ± 0.63 | 5 | −25.43 ± 0.62 | 5.79 ± 0.21 | – |
Herbivorous zooplankton | – | 3 | −30.75 ± 0.97 | 6.08 ± 0.81 | – | – | – | – |
Predatory zooplankton | – | 9 | −30.16 ± 1.35 | 10.05 ± 0.68 | 2 | −29.66 ± 0.08 | 9.89 ± 0.03 | – |
POM | – | 17 | −30.71 ± 1.63 | 4.02 ± 0.54 | 16 | −29.62 ± 1.42 | 4.16 ± 0.87 | – |
Detritus | – | 30 | −17.68 ± 4.09 | 3.25 ± 1.14 | – | – | – | – |
Emergent plants |
– | – | – | – | 15 | −25.72 ± 1.28 | 2.46 ± 2.92 | – |
Submerged plants |
– | 7 | −21.47 ± 5.76 | 3.00 ± 2.82 | 25 | −19.54 ± 3.62 | 0.93 ± 1.82 | – |
Filamentous algae |
– | – | – | – | 6 | −23.20 ± 1.52 | 1.63 ± 0.43 | – |
Because no long lived primary consumers were found in Lake Liambezi in order to baseline our datasets, variation in the isotope values (δ13C and δ15N) of basal resources sampled in both years were assessed by multivariate statistical analyses performed using the PRIMER package, version 6 with PERMANOVA (Clarke and Gorley,
The trophic structure of the fish community was then compared between 2011 and 2012 using six quantitative isotope metrics (Layman et al.,
The trophic structure of the fish community sampled in 2011 only was further resolved by calculating the SEAc of each taxonomic/feeding group, and the % of SEAc overlap between groups (as fishes were more comprehensively sampled in 2011). The SEAc and % overlap of individual species within important consumer groups were then calculated to elucidate interspecific trophic interactions and explore potential competition in the lacustrine fish community. The groups of species examined included the alestids, which have been a dominant component of the fish fauna in the lake since it filled, the tilapiine cichlids on which the fishery is based, generalist predators that include the highly abundant
To aid in interpreting the results of the stable isotope analyses, stomach contents were conducted the four most abundant, large piscivorous fish species in Lake Liambezi;
Dietary composition of the five study species was assessed by calculating the index of relative importance (IRI; Pinkas et al.,
where %
In 2011, 424 samples were collected for stable isotope analysis, comprised of three basal carbon sources, four general invertebrate groups and 30 fish species (
Stable δ13C-δ15N isotopic bi-plots of fish groups and their potential food sources from Lake Liambezi in 2011 and 2012. Data points represent the mean ± standard deviation for each group.
Overall, mixing model results for primary and secondary fish consumers showed that 58% of modeled fish species in 2011 and 87.5% in 2012 had substantial dietary POM contributions of >15%. In 2011 83% of fish species also had strong dietary contributions (>12.5%) of submerged plants. Briefly; topminnows and alestids relied almost exclusively on zooplankton and aquatic invertebrates in both years,
Proportional resource contributions to primary and secondary fish consumers as determined by Bayesian MixSIAR mixing models for 2011.
Proportional resource contributions to primary and secondary fish consumers as determined by Bayesian MixSIAR mixing models for 2012.
Both 2011 and 2012 data suggest that POM was the ultimate driver of the Lake Liambezi food web (either directly or indirectly), with three potential energy pathways by which basal resources were assimilated into the food web. Firstly, in 2011, the isotopic position of herbivorous zooplankton indicated that their diets likely consisted exclusively of POM. Secondly, aquatic invertebrates (including decapods in 2012) were similarly positioned, but demonstrated more variable δ13C values, indicating that while this diverse group relies primarily on POM, they likely also assimilate carbon from a range of other basal resources, including emergent plants and potentially their associated detritus and/or periphyton. The aquatic invertebrate group consisted mainly of benthic organisms, so their main source of POM likely settled out of the water column, possibly in the form of planktonic detritus (e.g., sinking phytoplankton). Thirdly, the relatively depleted values of δ15N and slightly enriched δ13C values (in 2012 only) of tilapiine cichlids relative to other fish species, suggest that although POM was a substantial contributor to tilapiine cichlid diet, considerable amounts of their dietary carbon were also derived from aquatic plants and detritus/periphyton compared to other consumers (
Stomach contents of fish species (no. of stomachs; % empty) and their length, by % number (
434–1,220 TL | 16 | ||||||
Fish | Fish remains | 23.53 | 8.27 | 6.35 | 5.50 | ||
Cichlidae | 76.47 | 91.73 | 20.63 | 94.50 | |||
195–386 TL | 35 | ||||||
Fish | Fish remains | 26.32 | 8.22 | 8.00 | 7.91 | ||
Cichlidae | 71.05 | 89.66 | 20.00 | 91.98 | |||
Alestidae | 2.63 | 2.12 | 0.80 | 0.11 | |||
120–302 TL | 14 | ||||||
Fish | Fish remains | 35.29 | 30.00 | 8.11 | 40.48 | ||
Cichlidae | 17.65 | 13.79 | 4.05 | 9.75 | |||
Alestidae | 41.18 | 53.45 | 6.76 | 48.88 | |||
Aquatic invertebrates | Insect remains | 5.88 | 2.76 | 1.35 | 0.89 | ||
90–273 FL | 137 | ||||||
Fish | Fish remains | 9.73 | 10.45 | 15.35 | 12.54 | ||
Cichlidae | 13.57 | 69.36 | 19.09 | 64.08 | |||
Alestidae | 1.36 | 10.83 | 2.07 | 1.02 | |||
Cyprinodontidae | 0.45 | 0.24 | 0.41 | 0.01 | |||
Aquatic invertebrates | Insect remains | 8.60 | 1.89 | 15.77 | 6.69 | ||
Ephemeroptera | 36.20 | 4.83 | 7.47 | 12.41 | |||
Trichoptera | 0.23 | 0.03 | 0.41 | 0.00 | |||
Coleoptera | 0.23 | 0.00 | 0.41 | 0.00 | |||
Hemiptera | 0.23 | 0.00 | 0.41 | 0.00 | |||
Odonata | 0.90 | 0.24 | 1.66 | 0.08 | |||
Diptera | 19.68 | 0.86 | 3.32 | 2.76 | |||
Decapoda | 1.13 | 0.37 | 1.24 | 0.08 | |||
Gastropoda | 0.23 | 0.02 | 0.41 | 0.00 | |||
Terrestrial invertebrates | Lepidoptera | 0.23 | 0.07 | 0.41 | 0.00 | ||
Orthoptera | 0.90 | 0.29 | 1.66 | 0.08 | |||
Araneae | 0.23 | 0.03 | 0.41 | 0.00 | |||
Insect eggs | 5.66 | 0.17 | 0.83 | 0.20 | |||
Detritus | 0.45 | 0.31 | 0.83 | 0.03 | |||
24–127 FL | 30 | ||||||
Fish | Fish remains | 4.19 | 20.05 | 20.51 | 7.88 | ||
Aquatic invertebrates | Insect remains | 9.95 | 27.11 | 46.15 | 27.09 | ||
Ephemeroptera | 2.62 | 4.33 | 7.69 | 0.85 | |||
Trichoptera | 2.09 | 4.10 | 7.69 | 0.75 | |||
Odonata | 0.52 | 1.67 | 2.56 | 0.09 | |||
Diptera | 53.93 | 18.73 | 41.03 | 47.22 | |||
Zooplankton | 18.85 | 0.75 | 25.64 | 7.96 | |||
Insect eggs | 4.71 | 12.99 | 23.08 | 6.47 | |||
Plant matter | 1.05 | 4.93 | 5.13 | 0.49 |
The average δ13C of tilapiine cichlids showed a 3‰ depletion in 2012, possibly indicating a shift to a more POM based diet. Further sampling of the tilapiine cichlids was carried out in 2014 to establish whether the shift to a lower δ13C diet was permanent. δ13C values did not differ significantly between years for
The NR and CR of the fish community in 2012 were higher than in 2011, suggesting that both the trophic length and range of basal resources used by the fish community in 2012 was greater. However, the average degree of trophic diversity (CD), was similar between years. Lower MNND and SDNND in 2011 indicate greater density and evenness of species packing in bi-plot space (
Stable isotope community metrics (mean with 95% CI in parentheses) comparing the trophic structure of fish communities sampled from Lake Liambezi in 2011 and 2012.
NR | 5.03 (4.43–5.66) | 5.67 (4.84–6.74) |
CR | 6.95 (5.59–8.89) | 7.95 (6.72–9.49) |
CD | 2.12 (1.88–2.38) | 2.05 (1.83–2.28) |
MNND | 0.87 (0.67–1.08) | 0.98 (0.80–1.18) |
SDNND | 0.54 (0.33–0.79) | 0.79 (0.53–1.06) |
SEAc | 11.93 (10.07–14.15) | 13.42 (11.89–15.23) |
Sample size ( |
259 | 212 |
The core isotopic niche areas (SEAc) of
Tilapiine cichlids, despite being the backbone of the Lake Liambezi gill net fishery, made up only 4% of the CPUE (kg net−1 night−1) (
The core isotopic niche area (SEAc) and percent overlap between fish groups in Lake Liambezi in 2011.
Alestids | 2.80 | 1.2 | 2.3 | 23.1 | 0.0 | 3.2 | 0.0 | 53.8 | |
Cyprinids | 4.47 | 1.9 | 55.1 | 45.5 | 41.9 | 0.0 | 5.6 | 0.0 | |
Benthic cichlids | 6.69 | 5.6 | 82.5 | 66.4 | 54.7 | 4.7 | 2.8 | 13.0 | |
Generalist predators | 6.78 | 56.0 | 69.0 | 67.2 | 34.1 | 8.2 | 0.0 | 55.7 | |
Mormyrids | 5.71 | 0.1 | 53.6 | 46.7 | 28.8 | 0.0 | 15.7 | 0.0 | |
Piscivores | 5.31 | 6.0 | 0.0 | 3.7 | 6.4 | 0.0 | 0.0 | 40.2 | |
Tilapiine cichlids | 13.77 | 0.0 | 17.3 | 5.9 | 0.0 | 37.8 | 0.0 | 0.0 | |
Topminnows | 3.64 | 70.0 | 0.0 | 7.1 | 29.9 | 0.0 | 27.5 | 0.0 |
The trophic level of the alestids
Of the four tilapiine cichlids,
The core isotopic niche area (SEAc) and percent overlap between (A) tilapiine cichlid species and (B) predatory fish species in Lake Liambezi in 2011.
8.9 | 35.7 | 0.1 | 12.0 | |||
4.2 | 16.9 | 0.0 | 0.0 | |||
11.4 | 0.1 | 0.0 | 49.6 | |||
8.1 | 10.9 | 0.0 | 35.3 | |||
2.73 | 0.0 | 3.7 | 31.7 | 42.7 | ||
3.41 | 0.1 | 42.2 | 0.0 | 6.1 | ||
5.83 | 7.9 | 72.1 | 11.6 | 0.0 | ||
5.77 | 67.0 | 0.0 | 11.5 | 50.3 | ||
3.55 | 55.7 | 6.4 | 0.0 | 31.0 |
The core niche areas of piscivores and generalist predators were examined together (
A diverse range of prey were recorded from full stomachs of
Identifiable items in full stomachs of
Stable isotopic values of POM indicated that it was composed primarily of freshwater phytoplankton (see Cloern et al.,
Carbon from phytoplankton and aquatic macrophytes was assimilated into the food web via three major pathways, one pelagic and two benthic. These are summarized visually in
Conceptual diagram of the food web in Lake Liambezi, illustrating the flow of energy through three major food chains, and their integration by generalist predators and piscivores in the mature lacustrine fish community. *Herbivores and detritivores incorporate all the tilapiine cichlids. All fish images are ©NRF-SAIAB.
In the pelagic food web phytoplankton was assimilated directly by herbivorous zooplankton, such as calanoid copepods (Grosbois et al.,
Thus, the second major pathway by which basal carbon was assimilated into the food web was via aquatic invertebrates that feed primarily on detritus of planktonic origin or potentially on emergent macrophytes and associated macrophytic detritus and/or periphyton. Among the most important aquatic invertebrates in Lake Liambezi are diptera larvae, ephemeroptera, trichoptera, and odonata nymphs (Seaman et al.,
The third major pathway involves the tilapiine cichlids which include
While the three trophic pathways discussed above are by no means discrete (fishes may forage across pelagic and benthic food chains), predators occupying the highest trophic levels fully integrate all pathways (Vander Zanden and Vadeboncoeur,
Stomach contents and stable isotope analysis revealed a significant level of dietary overlap among the three piscivores
The use of the pelagic food chain, even if on a small scale, by
Conceptual diagram of the food web in the Zambezi River as described by Taylor et al. (
In summary, the investigations into trophic and food web structure supports the hypothesis that phytoplankton production supports a high amount of consumer biomass in Lake Liambezi, however substantial contributions by periphyton/emergent plants are also likely. These results add to the large body of evidence highlighting the importance of algal production sources to fishes, even where macrophytes appear to be the dominant source of primary production (Winemiller,
The datasets generated for this study are available on request to the corresponding author.
The animal study was reviewed and approved by South African Institute for Aquatic Biodiversity Animal Ethics Committee.
RP and OW: ideas, data collection, analysis, manuscript preparation, and funding. JH: ideas, analysis, and manuscript preparation. GT: ideas, data collection, and analysis.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
We gratefully acknowledge the Ministry of Fisheries and Marine Resources, Namibia, for granting permission to carry out this research and for providing technical and logistic support. We acknowledge use of infrastructure and equipment provided by the SAIAB Research Platform and the funding channelled through the NRF-SAIAB Institutional Support system. Special thanks to Denis Tweddle for logistical, technical and intellectual support. Thank you to Susan Abraham for drawing our stylized food web diagrams
The Supplementary Material for this article can be found online at: