Studies Of Marine Food Webs Research Articles

Diatoms and fatty acid production in Arctic and estuarine ecosystems—a reassessment of marine food webs, with a focus on the timing of shorebird migration

This review highlights diatoms and their production of fatty acids at Arctic ice edges and temperate estuaries as strategic in initiating high spring productivity. As important as their energy production is their synthesis de novo of omega-3 long-chain polyunsaturated fatty acids (LCPUFAs), which are bioactive molecules fundamental to maintaining ecosystem processes, and are necessary for reproduction and growth for the entire marine food web. Without these fatty acids, consumers can suffer poor reproduction and growth even with sufficient energy intake, and shorebirds may need LCPUFAs for nonstop long-hop migration. Timing of high energy fatty acid and LCPUFA production by diatoms coincides with growth and reproduction of consumer populations, with the arrival of seabirds in the Arctic and staging of shorebirds in estuaries. The switch from diatom production of carbohydrates to fatty acids is triggered by changes in chemical and physical environmental factors, which can be muted by factors such as climate change or habitat modification. Higher ocean temperatures and lower pH from climate change alters the ability of diatoms to make LCPUFAs, and habitat degradation reduces the numbers of diatoms in the area, subsequently reducing the amounts of LCPUFA produced. Changes in LCPUFA output could impact functionality of ice-edge and estuarine ecosystems, impacting shorebird migration and consumer productivity. Research is scarce on marine consumer reproduction and growth comparing quantity vs. quality of ingested saturated, monounsaturated, and omega-3 LCPUFAs, and nonexistent for seabirds and shorebirds. Future studies of marine food webs should include the role of diatoms and their contribution of not just energy, but also LCPUFAs to the food web.

Beyond trophic morphology: stable isotopes reveal ubiquitous versatility in marine turtle trophic ecology.

ABSTRACTThe idea that interspecific variation in trophic morphology among closely related species effectively permits resource partitioning has driven research on ecological radiation since Darwin first described variation in beak morphology among Geospiza.Marine turtles comprise an ecological radiation in which interspecific differences in trophic morphology have similarly been implicated as a pathway to ecopartition the marine realm, in both extant and extinct species. Because marine turtles are charismatic flagship species of conservation concern, their trophic ecology has been studied intensively using stable isotope analyses to gain insights into habitat use and diet, principally to inform conservation management. This legion of studies provides an unparalleled opportunity to examine ecological partitioning across numerous hierarchical levels that heretofore has not been applied to any other ecological radiation. Our contribution aims to provide a quantitative analysis of interspecific variation and a comprehensive review of intraspecific variation in trophic ecology across different hierarchical levels marshalling insights about realised trophic ecology derived from stable isotopes.We reviewed 113 stable isotope studies, mostly involving single species, and conducted a meta‐analysis of data from adults to elucidate differences in trophic ecology among species. Our study reveals a more intricate hierarchy of ecopartitioning by marine turtles than previously recognised based on trophic morphology and dietary analyses. We found strong statistical support for interspecific partitioning, as well as a continuum of intraspecific trophic sub‐specialisation in most species across several hierarchical levels. This ubiquity of trophic specialisation across many hierarchical levels exposes a far more complex view of trophic ecology and resource‐axis exploitation than suggested by species diversity alone. Not only do species segregate along many widely understood axes such as body size, macrohabitat, and trophic morphology but the general pattern revealed by isotopic studies is one of microhabitat segregation and variation in foraging behaviour within species, within populations, and among individuals.These findings are highly relevant to conservation management because they imply ecological non‐exchangeability, which introduces a new dimension beyond that of genetic stocks which drives current conservation planning.Perhaps the most remarkable finding from our data synthesis is that four of six marine turtle species forage across several trophic levels. This pattern is unlike that seen in other large marine predators, which forage at a single trophic level according to stable isotopes. This finding affirms suggestions that marine turtles are robust sentinels of ocean health and likely stabilise marine food webs. This insight has broader significance for studies of marine food webs and trophic ecology of large marine predators.Beyond insights concerning marine turtle ecology and conservation, our findings also have broader implications for the study of ecological radiations. Particularly, the unrecognised complexity of ecopartitioning beyond that predicted by trophic morphology suggests that this dominant approach in adaptive radiation research likely underestimates the degree of resource overlap and that interspecific disparities in trophic morphology may often over‐predict the degree of realised ecopartitioning. Hence, our findings suggest that stable isotopes can profitably be applied to study other ecological radiations and may reveal trophic variation beyond that reflected by trophic morphology.

A hyperiid amphipod acts as a trophic link between a scyphozoan medusa and juvenile Chinook Salmon

Gelatinous zooplankton (GZ) can impact productivity of marine ecosystems through competition with small pelagic fish and predation on early life history stages of species from multiple trophic levels. Nevertheless, GZ do not always represent ‘trophic dead ends.’ Some predators directly consume GZ, and many species host parasitoids which in turn are prey for other organisms. We characterized trophic relationships between the fried-egg jellyfish Phacellophora camtschatica, its hyperiid amphipod parasite (Hyperia medusarum), and juvenile Chinook Salmon Oncorhynchus tshawytscha in the Salish Sea. Hyperia medusarum occurred in 29–47% of Chinook Salmon stomachs over 3 years and were observed in high abundance on P. camtschatica medusae (mean = 428 individuals per medusa). Light and transmission electron microscopy confirmed the presence of morphologically similar nematocysts in the foreguts of H. medusarum from both medusae and Chinook Salmon stomachs. Occurrence of H. medusarum in Chinook Salmon diets was also positively related to an index of P. camtschatica abundance. Chinook Salmon stomachs contained almost exclusively mature female H. medusarum while males and juveniles were common on medusae. Size and sex ratio differences between hyperiids in Chinook Salmon diets and on medusae could reflect predator selectivity or sex and/or life-stage specific differences in H. medusarum behavior. Our results support previous speculation that GZ abundance may facilitate predation on hyperiids by Pacific Salmon. Hyperiid-mediated energy flow from GZ to fish is not limited to medusa-associated fish species and should be considered in studies of marine food webs.

Grazing Impact of the Copepod Calanus sinicus on Phytoplankton in the Northern East China Sea in Late Spring

We investigated the feeding habits of Calanus sinicus during its four developmental stages as copepodite 4 (CIV), copepodite 5 (CV), adult males and females in early June 2015 at 12 sampling stations along the southern coast of Korea to the northern East China Sea, to better understand the role of C. sinicus in controlling phytoplankton stocks. Ingestion rate, daily ration as body carbon, population ingestion rate, and grazing impact were estimated using the gut pigment method. The mean biomass of CVs was the greatest (13.5 mg C m–3) and that of adult males was the lowest (0.7 mg C m–3). The ingestion rate per C. sinicus individual tended to increase with developmental stage, with the highest rate in adult females (519 ng chl ind–1 d–1) and the lowest rate in CIVs (305 ng chl ind–1 d–1). A significant correlation was found between ingestion rate and temperature, but not salinity or chlorophyll-a concentration. The daily ration of C. sinicus as body carbon significantly decreased with increased body weight, with the highest value found in CIVs (66.4%) and the lowest value in adult males (30%). Despite the high ingestion rate of the adults, the mean grazing impact of C. sinicus on phytoplankton biomass, in terms of chlorophyll-a concentration, was the highest in CVs (2.6%), followed by CIVs and adult females, and was the lowest in adult males (0.1%). The higher grazing impact of copepodites than adults underscores the importance of evaluating copepodite stages in the feeding studies of marine food webs.

Selection of isotopic baselines in marine ecosystems

Stable isotope analysis has been widely used in marine food web studies. An appropriate isotopic baseline is essential for calculating diet or trophic position of marine organisms when using stable isotopic data. This paper provided an overview of the selection of isotopic baselines for four ty-pical marine ecosystems, i.e. estuary and bay, neritic zone, oceanic zone, and deep sea. The interferential factors of baseline selection and the significance of compound specific stable isotope in minimizing the effects of temporal-spatial variations of isotopic baseline were summarized, and the issues needed to be solved in this field and several directions for further research were presented. It would provide a beneficial reference for further research on stable isotope ecology in marine ecosystems.

Setting the stage for a global-scale trophic analysis of marine top predators: a multi-workshop review

Global-scale studies of marine food webs are rare, despite their necessity for examining and understanding ecosystem level effects of climate variability. Here we review the progress of an international collaboration that compiled regional diet datasets of multiple top predator fishes from the Indian, Pacific and Atlantic Oceans and developed new statistical methods that can be used to obtain a comprehensive ocean-scale understanding of food webs and climate impacts on marine top predators. We loosely define top predators not as species at the apex of the food web, but rather a guild of large predators near the top of the food web. Specifically, we present a framework for world-wide compilation and analysis of global stomach-contents and stable-isotope data of tunas and other large pelagic predatory fishes. To illustrate the utility of the statistical methods, we show an example using yellowfin tuna in a “test” area in the Pacific Ocean. Stomach-contents data were analyzed using a modified (bagged) classification tree approach, which is being prepared as an R statistical software package. Bulk δ15N values of yellowfin tuna muscle tissue were examined using a Generalized Additive Model, after adjusting for spatial differences in the δ15N values of the baseline primary producers predicted by a global coupled ocean circulation-biogeochemical-isotope model. Both techniques in tandem demonstrated the capacity of this approach to elucidate spatial patterns of variations in both forage species and predator trophic positions and have the potential to predict responses to climate change. We believe this methodology could be extended to all marine top predators. Our results emphasize the necessity for quantitative investigations of global-scale datasets when evaluating changes to the food webs underpinning top ocean predators under long-term climatic variability.

Revisiting the use of δ15N in meso-scale studies of marine food webs by considering spatio-temporal variations in stable isotopic signatures – The case of an open ecosystem: The Bay of Biscay (North-East Atlantic)

Most of the recent framework directives and environmental policies argue for the development and the use of indicators – notably trophodynamic indicators – that should be able to follow ecosystems’ evolution in space and time, particularly under anthropogenic perturbations. In the last decades, the use of stable carbon and nitrogen isotopes ratios has increased exponentially, particularly in studies of marine ecosystems’ trophic structure and functioning. This method is principally based on the assumption that the isotopic composition of a consumer directly reflects that of its food. Nevertheless, few studies have attempted to define the limits of this tool, before using it and drawing ecological conclusions from isotopic analysis. This study aimed to assess the importance of considering spatio-temporal variations in isotopic signatures of consumers when using δ13C and especially δ15N values in open ecosystems with complex food webs, using the Bay of Biscay (North-East Atlantic) as a case study. To this end, more than 140 species from this marine ecosystem were analysed for the isotopic signatures in their muscle tissue. They were sampled from coastal to oceanic and deep-sea areas and at different latitudes, to evaluate spatial variations of isotopic signatures. Selected species were also sampled over several years and in two seasons to account for inter-annual and seasonal variations. In the Bay of Biscay temperate ecosystem, which is subject to both coastal and oceanic influences – two main river inputs and upwelling areas – , δ13C and δ15N values significantly decreased from inshore to offshore species, and to a lesser extent from benthic to pelagic organisms. River discharges appeared to be the first factor influencing δ13C and δ15N values in consumers. From the important spatial variations detected in δ15N values in particular, we suggest that in such contrasted ecosystem, nitrogen isotopic ratios may also be revisited as an indicator of the feeding area. Moreover, we demonstrate that several baselines should be used when calculating trophic levels from δ15N values. From the temporal variations detected, we recommend concentrating on a short time scale for the sampling most organisms.

Challenges using stable isotopes for estimating trophic levels in marine amphipods

In marine food web studies, stable isotopes of nitrogen (δ15N) and carbon (δ13C) are widely used to estimate organisms’ trophic levels (TL) and carbon sources, respectively. For smaller organisms, whole specimens are commonly analyzed. However, this “bulk method” involves several pitfalls since different tissues may fractionate stable isotopes differently. We compared the δ15N and δ13C values of exoskeleton versus soft tissue, in relation to whole specimens, of three common Arctic amphipods in Svalbard waters: the benthic Anonyx nugax, the sympagic (ice-associated) Gammarus wilkitzkii and the pelagic Themisto libellula. The δ15N values of the exoskeletons were significantly lower than those of the soft tissues for A. nugax (10.5 ± 0.7‰ vs. 15.7 ± 0.7‰), G. wilkitzkii (3.3 ± 0.3‰ vs. 8.3 ± 0.4‰) and T. libellula (8.6 ± 0.3‰ vs.10.8 ± 0.3‰). The differences in δ13C values between exoskeletons and soft tissues were insignificant, except for A. nugax (−21.2 ± 0.2‰ vs. −20.3 ± 0.2‰, respectively). The δ15N values of whole organisms were between those of the exoskeletons and the soft tissues, being similarly enriched in 15N as the exoskeletons (except G. wilkitzkii) and depleted in 15N by 1.2–3.7‰ compared to the soft tissues. The δ15N-derived TLs of the soft tissues agreed best with the known feeding preferences of the three amphipods, which suggest a potential underestimation of 0.5–1.0 TL when stable isotope analyses are performed on whole crustaceans with thick exoskeletons. The insignificant or small differences in δ13C values among exoskeletons, soft tissues and whole specimens, however, suggest low probability for misinterpretations of crustaceans’ primary carbon source in marine ecosystems with distinctly different δ13C-carbon sources.

Preservation methods alter stable isotope values in gelatinous zooplankton: implications for interpreting trophic ecology

Jellyfish are increasingly topical within studies of marine food webs. Stable isotope analysis represents a valuable technique to unravel the complex trophic role of these long-overlooked species. In other taxa, sample preservation has been shown to alter the isotopic values of species under consideration, potentially leading to misinterpretation of trophic ecology. To identify potential preservation effects in jellyfish, we collected Aurelia aurita from Strangford Lough (54o22′44.73″N, 5o32′53.44″W) during May 2009 and processed them using three different methods prior to isotopic analysis (unpreserved, frozen and preserved in ethanol). A distinct preservation effect was found on δ15N values: furthermore, preservation also influenced the positive allometric relationship between individual size and δ15N values. Conversely, δ13C values remained consistent between the three preservation methods, conflicting with previous findings for other invertebrate, fish and mammalian species. These findings have implications for incorporation of jellyfish into marine food webs and remote sampling regimes where preservation of samples is unavoidable.

Contrasting patterns of individual specialization and trophic coupling in two marine apex predators

1. Apex predators are often assumed to be dietary generalists and, by feeding on prey from multiple basal nutrient sources, serve to couple discrete food webs. But there is increasing evidence that individual level dietary specialization may be common in many species, and this has not been investigated for many marine apex predators. 2. Because of their position at or near the top of many marine food webs, and the possibility that they can affect populations of their prey and induce trophic cascades, it is important to understand patterns of dietary specialization in shark populations. 3. Stable isotope values from body tissues with different turnover rates were used to quantify patterns of individual specialization in two species of 'generalist' sharks (bull sharks, Carcharhinus leucas, and tiger sharks, Galeocerdo cuvier). 4. Despite wide population-level isotopic niche breadths in both species, isotopic values of individual tiger sharks varied across tissues with different turnover rates. The population niche breadth was explained mostly by variation within individuals suggesting tiger sharks are true generalists. In contrast, isotope values of individual bull sharks were stable through time and their wide population level niche breadth was explained by variation among specialist individuals. 5. Relative resource abundance and spatial variation in food-predation risk tradeoffs may explain the differences in patterns of specialization between shark species. 6. The differences in individual dietary specialization between tiger sharks and bull sharks results in different functional roles in coupling or compartmentalizing distinct food webs. 7. Individual specialization may be an important feature of trophic dynamics of highly mobile marine top predators and should be explicitly considered in studies of marine food webs and the ecological role of top predators.

Marine environmental monitoring programmes in South Africa: a review

South Africa uniquely lies at the junction of two major currents, the Agulhas and the Benguela. The waters overlying the continental shelf exhibit exceptionally high short-, medium- and long-term (days to inter-decadal) variability compared with most other shelf areas, and strongly contrasting oceanographic conditions are observed on the east and west coasts. South Africa is rich in fisheries resources and associated environmental data collected over more than a century. The South African marine scientific community has a history of multidisciplinary studies of marine foodwebs, from the driving forces such as wind, currents and solar heating, to the top predators, with the development of kelp bed, sub-tidal reefs and estuarine ecosystem studies in the 1970s; the Benguela Ecology Programme, which ran through four successive five-year stages, focused on the pelagic marine resources. Various approaches have been used to observe the continental shelf at different time and space scales, including: macroscale but frequent satellite imagery, mesoscale environmental and fishery surveys, dedicated crossshelf transects in key areas, measurements of dynamic processes, use of moored buoys and coastal weather stations, and integrated monitoring approaches, including modelling and simulation studies. Between 30 and 50 years of comprehensive marine data now exist, which are proving useful in the application of an ecosystem approach to fisheries monitoring and management, as decadal changes become discernible. These observations need to continue; even though the single-species stock assessment and operational management procedures have not yet formally used environmental factors for fisheries management advice, they help us to understand the factors affecting fish population fluctuations and early life histories and to identify large-scale regime shifts where marine trophic structure and functioning alter to a new state.

Depth-dependence in stable isotope ratio δ 15N of benthic POM consumers: The role of particle dynamics and organism trophic guild

The stable nitrogen isotope ratio (δ 15N) is an established indicator of trophic hierarchy in marine food-web studies. Most of these studies presume that spatial variation in the primary food source is negligible, although a water-depth-related increase in δ 15N of particulate organic matter (POM) has been found in many systems. We used the high-Antarctic Weddell Sea shelf and slope ecosystem to test whether such a depth-related change in δ 15N is reflected at higher trophic levels, i.e., benthic consumers of POM. In suspension feeders (SF) we found a significant increase in δ 15N with water depth of up to 9.8‰, whereas in deposit feeders (DF) a depth effect was barely detectable. Particle-size preferences of the two feeding guilds combined with particle-size-dependent sinking velocities and biogeochemical reworking of POM are discussed as the major causes of these differences. It is essential to marine food-web studies to take into account the general depth effect on POM δ 15N as well as potential feeding-guild-specific differences in the response of POM consumer tissue δ 15N to avoid serious bias and misinterpretation of stable-isotope-based trophic information.

Sample preparation effects on stable C and N isotope values: a comparison of methods in Arctic marine food web studies

We compared effects of different sample preparation techniques on the stable carbon and nitrogen isotope values of fish muscle, whole crustaceans and particulate organic matter (POM). Comparisons were also made to untreated (i.e. dried and homogenised) samples. Relatively carbon- ate-rich samples treated with weak acid (0.1 N HCl), either by quickly wetting or acid dampening, were on average 1.3‰ more enriched in 13 C than duplicates soaked in 2 N HCl for 5 min, indicating incomplete carbonate removal with the weaker acid. In comparison, no differences in δ 15 N values were found between acid treatments, and a following water rinse had no effect on the δ 13 C or δ 15 N values. Chloroform-methanol (2:1 by volume) extraction overnight removed less lipids than Soxhlet extraction with 7% methanol in dichloromethane for 2 h, resulting in ~1.2‰ difference in δ 13 C values between treatments of lipid-rich duplicates. Different lipid-extraction methods did not lead to consis- tent differences in δ 15 N values, however. Depending on the lipid and carbonate content, untreated samples were depleted in 13 C by 0.8 to 4.4‰ and in 15 N by 0.6 to 1.4‰ compared to treated dupli- cates. We conclude that δ 13 C and δ 15 N values of samples with low lipid and carbonate content are highly comparable among studies regardless of pre-treatment methods, whereas the δ 13 C values of relatively lipid- and/or carbonate-rich samples must be carefully considered based on the pre- treatment applied to samples. In comparison, δ 15 N values are relatively robust to differences in car- bonate and lipid-removal methods, and δ 15 N values of untreated vs. carbonate- and lipid-treated samples are comparable within ±1.0‰.

Causes of sulfur isotope variability in the seagrass, Zostera capricorni

Sulfur has been proposed as a useful element to employ in addition to carbon and nitrogen in stable isotope studies of marine food webs, but variability in δ 34S of primary producers may prevent food web resolution. δ 34S values in green leaves of the seagrass, Zostera capricorni, showed considerable variability (12.7–17.6‰) in a survey in Moreton Bay, Australia. We demonstrated that δ 34S values were correlated with sediment organic matter (OM) content and height of seagrass on the tidal gradient, but these relationships were opposite to those expected from work elsewhere. In our survey, δ 34S values were relatively depleted at sites higher on the shore and with lower OM content. We did find the expected relationship of depleted δ 34S values where sediment porewater sulfide concentrations were higher. Any influence of OM content on δ 34S values would have been confounded in the survey by the relationship between height on shore and OM content itself. We separated the effects of height and OM content by creating the following treatments at one height on the shore: (1) OM added, (2) procedural control, and (3) untouched control. δ 34S values of seagrass in OM added plots were significantly depleted (5.6‰) relative to procedural (10.1‰) and untouched (11.0‰) controls 8 weeks after the manipulation. This demonstrated that OM content on its own does have the expected effect on δ 34S values of seagrass, so in the initial survey another factor, probably related to height on shore, must have overridden the influence of OM content. Seagrass roots are able to exude excess oxygen produced during photosynthesis, reoxidising sulfides in surrounding porewater. We demonstrated that the above and below-ground biomass of seagrass was higher low on the shore, and contend that higher seagrass productivity low on the shore results in greater reoxidation of sulfides and leads to more enriched δ 34S values of seagrass.

Sulfur stable isotopes separate producers in marine food-web analysis.

Ecological applications of stable isotope analysis rely on different producers having distinct isotopic ratios to trace energy and nutrient transfer to consumers. Carbon (C) and nitrogen (N) are the usual elements analysed. We tested the hypothesis that producers unable to be separated using C and N would be separated by sulphur (S), by reviewing estuarine and marine food web studies using all three elements (total of 836 pairwise comparisons between producers). S had a wider range of values across all producers than C and N (S: 34.4, C: 23.3, N: 18.7 per thousand ), and a higher mean difference among producers (S: 9.3, C: 6.5, N: 3.3 per thousand ). We varied from 1 to 10 per thousand the distance producers must be apart to be considered separate. For each of these gap distances, S-separated producers tied on C and N in 40% or more of cases. Comparing the three elements individually, S had fewer tied pairs of producers for any gap distance than C or N. However, S also has higher within-producer variability. Statistical tests on simulated data showed that this higher variability caused S to be less effective than C for analysing differences among mean producer values, yet mixing models showed that S had the smallest confidence intervals around mean estimates of source contributions to consumers. We also examined the spatial and temporal scales over which S isotope signatures of the saltmarsh plant Spartina alterniflora varied. Differences between samples taken within tens of metres were smallest, but between samples hundreds of metres apart were as different as samples thousands of kilometres apart. The time between samples being taken did not influence S signatures. Overall, the use of S is recommended because it has a high probability of distinguishing the contribution of different producers to aquatic food webs. When two elements are employed, the combination of S and C separates more producers than any other combination.

Indirect effects in complex ecosystems: recent progress and future challenges

Indirect effects are fundamental to the biocomplexity of ecological systems, and provide severe challenges to predicting the impacts of environmental change. Interest in indirect effects has expanded exponentially over the past 20 years. Indirect effects arise when direct interactions mediated by changes in density share a species, when species change the interaction between individuals of other species, or both. Past work, including many studies of marine food webs, has primarily documented the existence of indirect effects and how particular examples arise. Future challenges include (1) developing methods for the systematic detection of indirect effects, (2) documenting the functions describing different classes of interaction modifications, (3) exploring methods to predict indirect effects, including measurement of interaction strengths among species, (4) integrating time-scale differences into the theory of indirect effects, and (5) linking indirect effects and environmental variability. Ecologists are not alone in dealing with complex systems. Consequently, progress may be facilitated by exploring approaches developed in other scientific disciplines oriented toward complex systems.