The variability in zooplankton fatty acid composition may be an indicator of larval fish habitat quality as fatty acids are linked to fish larval growth and survival. We sampled an anadromous fish nursery, the Chowan River, during spring of 2013 in order to determine how the seston fatty acid composition varied in comparison with the zooplankton community composition and fatty acid composition during the period of anadromous larval fish residency. The seston fatty acid profiles showed no distinct pattern in relation to sampling time or location. The mesozooplankton community composition varied spatially and the fatty acid profiles were typical of freshwater species in April. The Chowan River experienced a saltwater intrusion event during May, which resulted in brackish water species dominating the zooplankton community and the fatty acid profile showed an increase in polyunsaturated fatty acids (PUFA), in particular eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA). The saltwater intrusion event was followed by an influx of freshwater due to high precipitation levels in June. The zooplankton community composition once again became dominated by freshwater species and the fatty acid profiles shifted to reflect this change; however, EPA levels remained high, particularly in the lower river. We found correlations between the seston, microzooplankton and mesozooplankton fatty acid compositions. Salinity was the main factor correlated to the observed pattern in species composition, and fatty acid changes in the mesozooplankton. These data suggest that anadromous fish nursery habitat likely experiences considerable spatial variability in fatty acid profiles of zooplankton prey and that are correlated to seston community composition and hydrodynamic changes. Our results also suggest that sufficient prey density as well as a diverse fatty acid composition is present in the Chowan River to support larval fish production.
Estuaries are considered important nursery habitat for many ecologically and commercially important fish and invertebrates (
The quality (chemical composition) of zooplankton prey can influence fish growth, development, and survival (
Fatty acids are present in estuaries as a result of
Zooplankton community composition in estuaries has been intensely studied and abiotic factors are thought to structure zooplankton communities (
Here we explore the species composition and variability in fatty acid composition of the lower food web at the freshwater/saltwater interface of an estuarine fish nursery, the Chowan River, North Carolina, USA. The Chowan River is considered a critical habitat for larval and juvenile blueback herring (
The overall goal of our study was to determine if species and fatty acid composition of the lower food web could be used to indicate habitat quality of an estuarine fish nursery. In order to achieve this goal, we examined the spatial and temporal variability in species composition of microzooplankton and mesozooplankton as well as the fatty acid composition of the seston, microzooplankton, and mesozooplankton during the period of larval fish residency in the Chowan River. Our specific objectives were to determine: (1) if differences in the species composition and fatty acid composition were present in the system; (2) if so, were there patterns in species composition and fatty acid composition in time and space; (3) if particular species were related to the species composition patterns and if particular fatty acids were related to the fatty acid composition patterns; (4) if changes in species and fatty acid composition were related to changes in salinity dynamics; (5) if patterns in fatty acid composition correlated across trophic levels. We hypothesized that species composition would be related to salinity and that fatty acid profiles of micro- and mesozooplankton would relate to species composition and would reflect that of the seston. If supported, this would suggest that the quality of the larval fish forage, based on fatty acids, could be used to assess fish nursery quality.
The Chowan River is one of the largest tributaries that drains into the Albemarle Sound (
Map data: ESRI, HERE, DeLorme, MapmyIndia, OpenStreetMap contributors, GIS user community.
Vertical profiles of temperature (°C) and salinity were measured with a conductivity, temperature, and depth sensor (CTD, Yellow Springs Instruments, Castaway). Water samples were collected at a depth of 3 m with a Niskin water sampler.
Water depths ranged from 5.27 to 7.56 m during zooplankton sampling. Two horizontal net tows were made with 0.5 m diameter nets of two different mesh sizes (60 and 200 µm). Two mesh sizes were used in order to generate an adequate representation of the zooplankton for the size range >60 µm. The zooplankton samples between 60 and 200 µm are designated microzooplankton and the >200 µm zooplankton samples are designated mesozooplankton throughout the remainder of the paper. The zooplankton net was towed obliquely through the water for 1 min (species composition) and 2 min (fatty acid composition) at an average boat speed of 0.75 m s−1. The volume filtered was calculated using the volume of a cylinder (
Samples were filtered through a sieve (60 or 200 µm) to remove the sugar formalin solution, and then added to a beaker with a known volume of water. A total of three subsamples (2 mL per subsample for microzooplankton and 5 mL per subsample for mesozooplankton) were analyzed for community composition using a Hensen-Stempel pipette. Organisms were identified using a dissecting microscope and enumerated using a Ward counting wheel. The zooplankton were identified to genus except for the freshwater copepods that were identified to order. Copepod nauplii were grouped together because identification can be difficult at this stage (
The water samples (300 mL) were concentrated on a 0.7 µm Whatman™ GF/F filter (47 mm diameter) and stored at −80 °C until ready to process, which constituted the seston material. The zooplankton samples were filtered through 60 and 200 µm sieves stacked to collect species based on size. Each sample was visually analyzed to determine the dominant species with a dissecting microscope, and detritus and phytoplankton were removed. The samples were concentrated on a GF/F filter (47 mm diameter) by mesh size (60, 200 µm), and stored at −80 °C until ready to process.
Total lipids were extracted with chloroform-methanol (2:1,
We performed a series of multivariate analyses to address our specific objectives. We used PERMANOVA a part of the PRIMER 6 statistical software package (
If PERMANOVA detected differences, we then generated separate, Bray-Curtis similarity matrices for microzooplankton species composition (60 µm mesh), mesozooplankton species composition (200 µm mesh), seston fatty acid composition, microzooplankton fatty acid composition, and mesozooplankton fatty acid composition. A separate cluster analysis was performed using PRIMER 6 in order to reveal patterns over time and space for each similarity matrix. Each individual sample was associated with a location in the river (upper, middle, lower) and month (April, May, June) and these labels were used for visualization of samples in the cluster dendrogram. Next, a similarity percentage analysis (SIMPER) test was used to compare similarities within groups and determine the species or fatty acids that contributed to each grouping from the cluster analysis (
We then wanted to determine if salinity and temperature were related to the observed patterns and we used redundancy analysis for this purpose (
Salinity was near zero (0.02–0.04) throughout the river in April. During May, salinities in the upper river remained low (0.07), but the water column became stratified in the middle and lower river, with salinities ranging from 0.28–1.66. The river returned to freshwater (0.04–0.08) again in June due to a tropical storm that brought heavy rains for a two-week period. North Carolina experienced the second wettest June since 1895 with rainfall that ranged from 15.2 to 19.05 cm in the study area (
There were significant differences between the overall microzooplankton and mesozooplankton community composition (PERMANOVA,
Dash marks represent species that were not included in the contribution of 70%.
Microzooplankton | Mesozooplankton | ||||
---|---|---|---|---|---|
Group 1 | Group 2 | Group 3 | Group 4 | Group 5 | |
Overall similarity | 91.18 | 80.18 | 84.39 | 57.16 | 52.52 |
Species | Percent composition | Percent composition | |||
Bosminidae | – | – | 17.26 | 34.25 | 12.20 |
– | – | – | – | 21.80 | |
Calanoida | – | – | – | 33.32 | 26.09 |
Cyclopoida | – | – | – | 10.24 | 9.07 |
– | – | 74.66 | – | – | |
Copepod nauplii | 10.60 | 41.61 | – | – | – |
Rotifer | 86.47 | 50.46 | – | – | – |
Dash marks represent fatty acids that were not included in the contribution of 70%. Group G had a sample size <2.
Seston | Microzooplankton | Mesozooplankton | ||||||||
---|---|---|---|---|---|---|---|---|---|---|
Group A | Group B | Group C | Group D | Group E | Group F | Group G | Group H | Group I | Group J | |
Overall similarity | 66.40 | 72.32 | 64.34 | 84.88 | 92.49 | 81.05 | N/A | 81.42 | 89.42 | 84.89 |
Fatty acids | Percent composition | Percent composition | Percent composition | |||||||
16:1 |
3.12 | 6.53 | – | – | – | 7.98 | – | 9.53 | – | 8.51 |
18:1 |
7.04 | 2.27 | 2.42 | 31.63 | 13.46 | – | 17.01 | 10.58 | – | – |
18:2 |
– | – | – | 12.15 | – | – | – | – | – | – |
18:3 |
2.37 | – | 3.33 | – | 8.43 | 6.80 | – | 6.14 | 10.65 | – |
18:4 |
– | – | – | – | 10.29 | – | – | – | 7.05 | – |
20:5 |
– | 1.55 | 2.44 | – | 11.72 | 9.91 | – | 11.24 | 13.84 | 16.40 |
22:6 |
– | – | 1.87 | – | – | 9.45 | – | – | 10.11 | 16.58 |
Three groups of mesozooplankton were differentiated at 50% similarity using cluster analysis (
A total of 24 specific fatty acids were found in all samples (
Three groups were designated at 60% similarity using cluster analysis for the seston fatty acid composition (
Three groups were designated at 70% similarity using cluster analysis for the microzooplankton fatty acid composition (
Four groups were designated by cluster analysis at 77% similarity for the mesozooplankton fatty acid composition (
Salinity was the main factor found to be correlated to observed patterns in the species composition of both microzooplankton and mesozooplankton (Redundancy,
We found temporal and spatial differences in the species and fatty acid composition of the lower food web that were mainly related to a salinity intrusion that occurred during the study period during May. Prior to the salinity intrusion, larval fish would have encountered a freshwater plankton assemblage that was dominated by rotifers, Bosminidae, and cylopoid copepods throughout the river. This assemblage was proportionally higher in EPA relative to DHA. During the salinity intrusion, the microzooplankton remained dominated by rotifers; however, the mesozooplankton community became dominated by the copepod
The seston fatty acid composition consisted mainly of saturated fatty acids. Seston from freshwater and estuarine systems typically has a large percentage of SFA and this fraction has been attributed to detrital input, as opposed to originating from phytoplankton (
We did not examine the seston composition directly by counting phytoplankton cells or examining pigment concentrations, thus we were unable to attribute the origin of particular fatty acids to phytoplankton or other sources. However, we were able to use the available literature to identify potential indicators of fatty acid origin. The top four fatty acids by percent composition varied by group, but 16:1ω-7, 18:1ω-9, 18:2 ω-6, and ALA were the most prevalent. Potential phytoplankton sources for these fatty acids may be diatoms, which have been shown to have increased 16:1ω-7 and EPA in both freshwater and marine systems (
The microzooplankton fatty acid profiles were different throughout the sampling period with a change from decreased omega-3s to increased omega-3s in the system. This suggests a switch in microzooplankton diet had occurred over the sampling period and two pathways appear to be present during the study. The April microzooplankton fatty acid profiles for all river sections had a high percentage of 18:1ω-9 and 18:2ω-6 suggesting that the microzooplankton could be consuming either terrestrial material or chlorophytes during this time. Two sites in April had an increase in omega-3 fatty acids (ALA, 18:4 ω-3, EPA, DHA), and this would suggest a different dietary pathway that was reduced in SFA, perhaps consisting of either smaller microzooplankton such as ciliates or phytoplankton such as diatoms and/or dinoflagellates (
The mesozooplankton fatty acid profiles throughout the river in April and in the upper river in May and June were defined by higher percentages of 16:1ω-7, 18:1ω-9, ALA, EPA, and DHA, and mixed mesozooplankton community consisting of cladoceran and copepods. These fatty acids profiles are similar to those found in freshwater systems that have a mixed zooplankton composition (
The relevance of the food web fatty acid composition can be determined by examining the potential feeding behavior of larval fish within the Chowan River nursery. Alewife and blueback herring start feeding on smaller cladocerans and copepods at about 6 mm total length (
The fish nursery present in the lower Chowan River may undergo significant changes during the critical time of larval fish growth and our results demonstrate how changes in the seston community may propagate through the food web. The results also highlight that additional information concerning the fatty acid composition of the zooplankton prey base for larval fish can provide insight into habitat quality, our stated goal.
I would like to thank S Lichti, C Krahforst, J Osborne, A Powell, M Baker, and E Diaddorio for help in the field collection. I would like to thank L Stratton, C Kolb, and R Pattridge for help in Dr. Jacques Rinchard’s lab in processing my fatty acid samples. I would like to thank Dr. Ariane Peralta for help with the improved statistical analysis, and two anonymous reviewers for comments, which helped to improve the manuscript.
Seston group | |||
---|---|---|---|
A (8) | B (5) | C (4) | |
14:0 | 6.6 ± 1.8 | 11.2 ± 5.1 | 7.6 ± 1.0 |
15:0 | 1.5 ± 1.5 | 1.3 ± 0.4 | 1.7 ± 0.3 |
16:0 | 47.7 ± 5.5 | 54.0 ± 5.1 | 50.8 ± 4.4 |
17:0 | 2.3 ± 0.4 | 2.7 ± 0.7 | 2.6 ± 0.2 |
18:0 | 14.2 ± 5.6 | 9.7 ± 1.2 | 11.4 ± 2.5 |
20:0 | 0.4 ± 0.3 | 0.3 ± 0.1 | 0.4 ± 0.2 |
16:1 |
1.2 ± 1.0 | 1.3 ± 0.6 | 1.6 ± 0.7 |
16:1 |
3.1 ± 1.9 | 6.3 ± 3.3 | 2.1 ± 1.9 |
18:1 |
7.0 ± 1.8 | 2.3 ± 0.8 | 2.4 ± 0.3 |
18:1 |
0.3 ± 0.2 | 0.1 ± 0.2 | 0.1 ± 0.1 |
20:1 | 0.1 ± 0.0 | 0.1 ± 0.0 | 0.2 ± 0.1 |
18:2 |
2.9 ± 4.2 | 0.6 ± 0.6 | 0.8 ± 1.2 |
18:3 |
2.4 ± 1.4 | 0.9 ± 0.5 | 3.3 ± 1.3 |
18:4 |
0.7 ± 1.1 | 0.1 ± 0.1 | 1.7 ± 1.4 |
20:2 |
0.5 ± 0.4 | 0.2 ± 0.2 | 0.7 ± 0.5 |
20:3 |
0.4 ± 0.1 | 0.4 ± 0.3 | 0.3 ± 0.2 |
20:4 |
0.9 ± 0.6 | 0.8 ± 0.4 | 0.8 ± 0.5 |
20:3 |
0.6 ± 0.3 | 0.4 ± 0.3 | 1.1 ± 0.6 |
20:4 |
0.6 ± 1.4 | 0.5 ± 0.3 | 2.3 ± 1.9 |
20:5 |
1.6 ± 1.1 | 1.6 ± 0.4 | 2.4 ± 1.7 |
22:5 |
0.7 ± 0.5 | 0.8 ± 0.8 | 1.2 ± 0.6 |
22:5 |
0.8 ± 0.6 | 0.7 ± 0.6 | 1.2 ± 0.7 |
22:6 |
1.4 ± 1.1 | 1.1 ± 0.6 | 1.9 ± 1.0 |
saturated fatty acids monounsaturated fatty acids polyunsaturated fatty acids.
Microzooplankton Groups | |||
---|---|---|---|
14:0 | 2.6 ± 0.5 | 3.7 ± 0.9 | 5.9 ± 1.1 |
15:0 | 0.3 ± 0.1 | 0.5 ± 0.2 | 1.1 ± 0.3 |
16:0 | 27.4 ± 3.0 | 24.5 ± 0.3 | 23.5 ± 3.4 |
17:0 | 0.4 ± 0.1 | 0.6 ± 0.0 | 1.2 ± 0.3 |
18:0 | 3.4 ± 0.8 | 3.4 ± 0.0 | 7.1 ± 0.3 |
20:0 | 1.8 ± 0.4 | 0.8 ± 0.1 | 0.2 ± 0.1 |
16:1 |
0.3 ± 0.1 | 0.8 ± 0.3 | 0.9 ± 0.6 |
16:1 |
2.2 ± 1.6 | 1.4 ± 0.1 | 7.1 ± 2.0 |
18:1 |
31.6 ± 5.3 | 13.5 ± 0.5 | 5.3 ± 3.1 |
18:1 |
0.7 ± 0.8 | 0.8 ± 0.2 | 1.9 ± 0.5 |
20:1 | 0.6 ± 0.2 | 0.8 ± 0.1 | 1.4 ± 0.6 |
18:2 |
12.2 ± 1.6 | 6.9 ± 0.9 | 2.8 ± 1.2 |
18:3 |
2.9 ± 1.3 | 8.4 ± 1.3 | 7.0 ± 1.7 |
18:4 |
3.2 ± 2.3 | 10.3 ± 1.5 | 2.8 ± 0.7 |
20:2 |
0.4 ± 0.1 | 0.5 ± 0.1 | 0.3 ± 0.1 |
20:3 |
0.1 ± 0.1 | 0.1 ± 0.0 | 0.2 ± 0.1 |
20:4 |
0.6 ± 0.7 | 0.4 ± 0.1 | 3.2 ± 0.5 |
20:3 |
0.3 ± 0.1 | 1.0 ± 0.2 | 0.4 ± 0.1 |
20:4 |
1.3 ± 0.4 | 2.8 ± 0.1 | 2.1 ± 0.3 |
20:5 |
5.0 ± 2.0 | 11.7 ± 1.4 | 9.9 ± 2.0 |
22:5 |
0.2 ± 0.2 | 1.0 ± 0.1 | 2.3 ± 0.9 |
22:5 |
0.2 ± 0.2 | 0.2 ± 0.1 | 1.9 ± 1.1 |
22:6 |
2.1 ± 1.5 | 5.6 ± 0.3 | 9.8 ± 3.2 |
saturated fatty acids monounsaturated fatty acids polyunsaturated fatty acids
Mesozooplankton groups | ||||
---|---|---|---|---|
14:0 | 4.5 | 5.4 ± 0.9 | 5.2 ± 1.1 | 5.1 ± 1.1 |
15:0 | 1.1 | 1.1 ± 0.4 | 0.7 ± 0.0 | 0.9 ± 0.1 |
16:0 | 29.7 | 24.4 ± 2.6 | 19.5 ± 1.3 | 22.0 ± 1.5 |
17:0 | 1.3 | 1.4 ± 0.4 | 1.0 ± 0.1 | 1.4 ± 0.3 |
18:0 | 11.2 | 7.7 ± 1.2 | 5.1 ± 0.3 | 6.8 ± 0.7 |
20:0 | 0.4 | 0.2 ± 0.0 | 0.2 ± 0.1 | 0.1 ± 0.1 |
16:1 |
0.3 | 0.9 ± 0.2 | 0.9 ± 0.4 | 0.8 ± 0.4 |
16:1 |
4.1 | 9.5 ± 2.2 | 6.2 ± 2.2 | 8.6 ± 2.2 |
18:1 |
17.0 | 10.6 ± 4.3 | 6.4 ± 1.2 | 4.0 ± 1.4 |
18:1 |
2.1 | 3.9 ± 1.7 | 2.4 ± 0.4 | 3.0 ± 1.1 |
20:1 | 0.3 | 0.1 ± 0.1 | 0.3 ± 0.1 | 0.2 ± 0.1 |
18:2 |
4.2 | 3.0 ± 0.9 | 5.1 ± 0.6 | 2.2 ± 0.7 |
18:3 |
2.9 | 6.1 ± 2.1 | 10.7 ± 1.5 | 5.1 ± 1.9 |
18:4 |
1.4 | 2.4 ± 0.8 | 7.1 ± 1.2 | 2.2 ± 0.4 |
20:2 |
0.2 | 0.2 ± 0.1 | 0.4 ± 0.1 | 0.2 ± 0.0 |
20:3 |
0.1 | 0.1 ± 0.0 | 0.1 ± 0.0 | 0.1 ± 0.0 |
20:4 |
3.7 | 4.2 ± 1.5 | 2.1 ± 0.6 | 2.5 ± 1.2 |
20:3 |
0.2 | 0.2 ± 0.1 | 0.5 ± 0.3 | 0.2 ± 0.1 |
20:4 |
0.8 | 0.6 ± 0.3 | 1.2 ± 0.6 | 0.8 ± 0.3 |
20:5 |
5.9 | 11.2 ± 2.4 | 13.8 ± 0.9 | 16.2 ± 0.6 |
22:5 |
0.4 | 0.4 ± 0.2 | 0.8 ± 0.2 | 1.8 ± 0.8 |
22:5 |
0.4 | 0.3 ± 0.2 | 0.4 ± 0.2 | 0.6 ± 0.3 |
22:6 |
7.3 | 5.7 ± 2.9 | 10.1 ± 2.8 | 15.1 ± 7.3 |
saturated fatty acids, monounsaturated fatty acids polyunsaturated fatty acids
The authors declare there are no competing interests.
The following information was supplied regarding data availability:
The raw data has been supplied as a