Trophic Step Research Articles

A missing trophic link: Contribution of the microbial loop to the estimation of the trophic position of pelagic consumers

AbstractTrophic position estimation has been a central issue in food web studies. Estimates using compound‐specific isotopic analyses of amino acids were generally based on the trophic enrichment of glutamic acid. However, this trophic position estimation mainly accounts for the trophic steps involving metazoa, as the isotopic fractionation of this amino acid is minimal at trophic steps within the microbial food web. Alternatively, trophic position estimates based on alanine seem to also reflect microbial trophic steps. The difference between these estimations can provide an index of the microbial food web contribution to the trophic position of a particular consumer. Here, we examined the differences between both trophic position estimates through a meta‐analysis of the published data over a large range of marine consumers. The results suggest that the microbial contribution to trophic position decreases as trophic position increases in the marine pelagic food web, showing the lowest values in top consumers. Ureotelic organisms showed the highest microbial contributions. The current data point to an upper limit for the estimation of this index at δ15N values of glutamic acid or alanine of ~ 18.5‰, or trophic positions of 3.9 or 4.7 for fish and ammoniotelic organisms, respectively. Under the stable isotope lens, bacteria and protists may play a key role in the estimation of trophic positions of consumers. However, uncertainties that related both to the microbial loop (e.g., metabolic bacterial pathways) and to metazoan consumers (e.g., influence of the gut microbiome) still obscure the establishment of clear quantitative links between microbial and metazoan food webs.

Temporal and spatial variability in the mesozooplankton community off the Falkland Islands (Southwest Atlantic)

Zooplankton communities vary in space and time. Their composition is strongly influenced by lower trophic levels that are dependent on the availability of light and nutrients. As all marine ecosystems are relying on zooplankton as intermediate trophic step between primary production and higher trophic levels, changes in the zooplankton community composition and biomass can cascade through the food web with important impacts on fish communities and through that on fisheries yields. An intense fisheries exist around the Falkland Islands in the SW Atlantic Ocean, around 51° S, but to the best of our knowledge, no previous study has to date investigated the seasonal variation in zooplankton community composition in these waters. We show that copepods (39.2%), the larvae of the anomurid Grimothea gregaria (33.1%) and euphausiids (10.9%) dominate the local mesozooplankton community by biomass. All species showed seasonal patterns, including ontogenetic behaviour of G. gregaria migrating to deeper waters with development, which were significantly explained by temperature (p < 0.001). While overall biomass significantly decreased with distance from shore (p < 0.001), mesozooplankton diversity was highest at 30 km from shore. The presented study is the first assessment of the mesozooplankton biomass off the Falkland Islands and provides a first baseline to aid future ecosystem studies in the context of ecosystem based fisheries management in the region.

An examination of the factors influencing the bioaccumulation of methylmercury at the base of the estuarine food web

Estuarine systems have received ongoing mercury (Hg) inputs from both point sources and regional contamination and have high legacy Hg in sediments. This is an environmental concern given that coastal seafood is an important vector for human exposure to methylmercury (MeHg). The base of the food chain represents the most important trophic steps for MeHg bioaccumulation. The magnitude of the uptake by phytoplankton, and their consumers, is influenced by many factors, in addition to sediment and water MeHg concentrations, that impact MeHg assimilation into phytoplankton and the trophic transfer to higher trophic levels, both benthic and pelagic. For forage fish, such as mummichogs (Fundulus heteroclitus), abiotic and biotic (bioenergetic) factors can influence their MeHg content, and diet is also important as they feed both on benthic and pelagic prey. Given that the importance of sediment MeHg versus pelagic MeHg sources has been debated, we updated a phytoplankton bioaccumulation model, and coupled this with a bioaccumulation model for MeHg concentration in mummichog tissue to examine the controlling factors for sites, from Maine to Maryland, USA, ranging widely in their Hg concentrations and other variables. The study highlighted the importance of DOC in modulating uptake into the pelagic food web, but also demonstrated the importance of diet in controlling mummichog MeHg. Finally, the relative importance of MeHg source - sediment or water column – was correlated with the level of Hg contamination. Sediment-derived MeHg was a more important source for highly Hg contaminated systems. As water column and sediment MeHg are not strongly correlated for the studied ecosystems, their importance as a source of MeHg to mummichogs varies with location. The study highlights the differences across ecosystems in MeHg bioaccumulation pathways, and that uptake into phytoplankton is an important variable controlling forage fish concentration.

Climate-driven zooplankton shifts cause large-scale declines in food quality for fish

Zooplankton are the primary energy pathway from phytoplankton to fish. Yet, there is limited understanding about how climate change will modify zooplankton communities and the implications for marine food webs globally. Using a trait-based marine ecosystem model resolving key zooplankton groups, we find that future oceans, particularly in tropical regions, favour food webs increasingly dominated by carnivorous (chaetognaths, jellyfish and carnivorous copepods) and gelatinous filter-feeding zooplankton (larvaceans and salps) at the expense of omnivorous copepods and euphausiids. By providing a direct energetic pathway from small phytoplankton to fish, the rise of gelatinous filter feeders partially offsets the increase in trophic steps between primary producers and fish from declining phytoplankton biomass and increases in carnivorous zooplankton. However, future fish communities experience reduced carrying capacity from falling phytoplankton biomass and less nutritious food as environmental conditions increasingly favour gelatinous zooplankton, slightly exacerbating projected declines in small pelagic fish biomass in tropical regions by 2100.

A Bayesian stable isotope mixing model for coping with multiple isotopes, multiple trophic steps and small sample sizes

Abstract We introduce a Bayesian stable isotope mixing model for estimating the relative contributions of different dietary components to the tissues of consumers within food webs. The model is implemented with the probabilistic programming language Stan. The model incorporates isotopes of multiple elements (e.g. C, N, H) for two trophic levels, when the structure of the food web is known. In addition, the model allows inclusion of latent trophic levels (i.e. for which no empirical data are available) intermediate between sources and measured consumers. Running the model in simulations driven by a real dataset from Finnish lakes, we tested the sensitivity of the posterior distributions by altering critical prior parameters and assumptions in the data‐generating process. Importantly, we found that the model estimations were particularly sensitive to the assigned prior value for ω (the fraction of H in aquatic consumer tissue that is derived from environmental water rather than diet) so that reliable empirical data for this parameter are required. When reliable information is not available for ω, we suggest that an uninformative prior should be used. The proposed model and inferences are suitable for studies where resources for collecting new data are limited, but useful prior information for each specific trophic level is available from earlier studies.

Reevaluating trophic discrimination factors (Δδ13C and Δδ15N) for diet reconstruction

AbstractStable isotope analysis is increasingly being used to assess diet and trophic positions of animals. Such assessments require estimates of trophic discrimination factors (TDFs)—offset between the isotopic composition of diet and animal tissues—with imprecise applications of TDFs leading to biased conclusions in resource use. Because TDFs are unavailable for most species, ecologists often apply values from taxonomically similar species or use trophic step increases of approximately 1‰ for carbon (TDF‐δ13C) and 3‰ for nitrogen (TDF‐δ15N). Such practices may yield inaccuracies since TDFs vary greatly, even within a species. To better understand the factors that influence TDFs, we conducted a meta‐analysis of TDF‐δ13C and TDF‐δ15N for mammals and quantified variation in relation to consumer type (herbivore, omnivore, carnivore) and diet source (C3‐based, C4‐based, marine‐based, mixture). Additionally, to guide TDF choice, we used an isotopic data set of small mammal tissues and diet items to assess how predicted dietary contributions vary with TDFs estimated using (1) taxonomic relatedness, (2) consumer type and diet source, or (3) values derived from wild animals eating natural diets. Our meta‐analysis revealed that metabolic routing and interactions between consumer class, dietary source, and the protein versus energy content of diets best explained variation in TDF‐δ13C values (−1.5‰ to 7.3‰), whereas consumer class best explained variation in TDF‐δ15N values (−0.5‰ to 7.1‰). Our test of methods to estimate TDFs indicated that ecologists should avoid relying on taxonomic relatedness when selecting TDF‐δ13C because mixed‐diet lab studies may produce misleading results for herbivores and omnivores. Additionally, field‐derived estimates could help fill TDF gaps where diets within a consumer class are absent. Overall, we suggest that using standard TDF trophic step values should be abandoned, because feeding studies are often poor proxies for natural diets, particularly for herbivores and omnivores. Instead, we make recommendations on how to select TDFs, along with a range of TDF‐δ13C and TDF‐δ15N values depending on diet source, consumer class, and tissue type. Use of these more refined recommendations and TDF values in isotopic assessments will improve estimates of diets and trophic interactions in natural systems, leading to a better understanding of ecological interactions and communities.

Reconstructed Paleodiets and Subsistence Strategies of the Central Ciscaucasian Population (1000 BC to 1000 AD), Based on Collagen Isotope Analysis of Bone Samples from the Kichmalka II Burial Ground

Settlement and economy patterns of the Iron Age and early medieval population of the Central North Caucasus evidence complex cultural processes in the region. The ecological approach including the evaluation of carbon and nitrogen isotopes in the local biota opens up new prospects in the study of environments, climate, anthropogenic effect, land use, and nutrition. We analyze the isotopic composition of collagen in 19 human and 11 animal bone samples from Kichmalka II—a cemetery successively used by the Koban people, those of the Sarmatian stage, and Alans. The isotopic composition of the Alanian sample indicates a heavy predominance of plants with the C3-type photosynthesis in the diet of humans and animals. People who lived during the Koban and Sarmatian stages consumed also C4-plants, such as common millet (Panicum miliaceum), suggesting the rise of the trophic step for carbon (Δδ13Chuman-animal). Statistically signifi cant differences in the isotopic composition of carbon were found within the Koban population, apparently evidencing two dietary models. The Δδ15Nhuman-animal values fall within the trophic step, mirroring a focus on meat and dairy products in the diet of all groups. Comparison with respective data on the Klin-Yar III cemetery revealed differences in isotopic signatures in the diet of both humans and domestic animals during the Koban period. The possible reason is climatic change in the Iron Age and the variable share of millet in the diet of the Koban people. The low proportion of δ15N (below 4 ‰) in the bone collagen of goat, sheep, and horse of the Alanian period may attest to vertical transhumance.

Zooplankton trophic structure and ecosystem productivity

The number of trophic steps within a plankton food web plays an important role in determining the energy available to support higher-level consumers by affecting trophic transfer efficiency (TE): fewer steps can enhance TE by decreasing respiration and predation losses. In this study, trophic structure within the zooplankton community was investigated using stable isotopes in size-fractionated mesozooplankton, and related to 2 biomass proxies related to TE: the normalized biomass size spectra (NBSS) and the ratio of zooplankton:phytoplankton biomass (log10(zoo:phyto)). Four regions were compared: the California Current Ecosystem (CCE—most productive), the Equatorial Pacific (EqP), the Costa Rica Dome (CRD) and the North Pacific Subtropical Gyre (NPSG—least productive). Compound-specific isotope analysis of amino acids confirmed large differences (~3‰) in the isotopic baseline among ecosystems. EqP and NPSG had low and distinct source δ15N values, while CRD/CCE had high and overlapping values. Trophic differences indicated that the CCE had the lowest number (0) of trophic differences within the 4 zooplankton size classes; NPSG and EqP had the highest number (3), and CRD was intermediate (1). NBSS slopes confirmed the CCE and NPSG as extremes and statistically different from each other. TE patterns estimated from log10(zoo:phyto) suggested EqP was the least efficient, while the other 3 ecosystems (despite large ranges in zooplankton and phytoplankton biomass) had similar TEs. The inverse relationship between food chain length and system productivity, a paradigm originally formulated for microbial food webs, holds for the mesozooplankton assemblage at the productivity extremes.

Kelp-Associated Microbes Facilitate Spatial Subsidy in a Detrital-Based Food Web in a Shoreline Ecosystem

Microbes are ubiquitous but our knowledge of their effects on consumers is limited in benthic marine systems. Shorelines often form hotspots of microbial and detritivore activity due to the large amounts of detrital macrophytes that are exported from other coastal ecosystems, such as kelp forests, and accumulate in these systems. Shoreline ecosystems therefore provide a useful model system to examine microbial-detritivore interactions. We experimentally test whether bacteria in the biofilm of kelp provide a bottom-up influence on growth and reproductive output of detritivores in shorelines where detrital kelp accumulates, by manipulating the bacterial abundances on kelp (Ecklonia radiata). The growth rates for both male and female amphipods (Allorchestes compressa) were greater in treatments containing bacteria than those in which bacteria were reduced through antibiotic treatment, and this effect was greater for males offered aged kelp. The proportions of ovigerous females were greater when reared on kelp with intact bacteria, indicating a more rapid reproductive development in the presence of more bacteria. Bacterial abundance had little to no influence on nutrient content and palatability of kelp, based on tissue toughness, nitrogen and carbon content and C:N ratio. Thus, the most likely pathway for a microbial effect on detritivores was through feeding on kelp-associated bacteria. Regardless of the pathway, kelp-associated microbes have a strong influence on the fitness of a highly abundant detritivore that feeds preferentially on E. radiata in shoreline systems, and therefore form a hidden trophic step in this “brown” food web and a hotspot of secondary production.

Fatty acid accumulation in feeding types of a natural freshwater fish population

Fatty acids are widely used to study trophic interactions in food web assemblages. Generally, it is assumed that there is a very small modification of fatty acids from one trophic step to another, making them suitable as trophic biomarkers. However, recent literature provides evidence that many fishes possess genes encoding enzymes with a role in bioconversion, thus the capability for bioconversion might be more widespread than previously assumed. Nonetheless, empirical evidence for biosynthesis occurring in natural populations remains scarce. In this study, we investigated different feeding types of perch (Perca fluviatilis) that are specialized on specific resources with different levels of highly unsaturated fatty acids (HUFAs), and analyzed the change between HUFA proportions in perch muscle tissue compared to their resources. Perch showed matching levels to their resources for EPA, but ARA and especially DHA were accumulated. Compound-specific stable isotope analyses helped us to identify the origin of HUFA carbon. Our results suggest that perch obtain a substantial amount of DHA via bioconversion when feeding on DHA-poor benthic resources. Thus, our data indicate the capability of bioconversion of HUFAs in a natural freshwater fish population.

Trophic indices for micronektonic fishes reveal their dependence on the microbial system in the North Atlantic

The importance of microbes for the functioning of oceanic food webs is well established, but their relevance for top consumers is still poorly appreciated. Large differences in individual size, and consequently in growth rates and the relevant spatial and temporal scales involved, make the integration of microorganisms and large metazoans in a common food web framework difficult. Using stable isotopes, this study estimated the trophic position of 13 species of micronektonic fishes to examine the microbial and metazoan contribution to mid trophic level consumers. Vertically migrant species displayed higher trophic positions than non-migrant species in all depth layers. The estimated trophic positions agreed well with those from the literature, but all species displayed mean increases between 0.5 and 0.8 trophic positions when taking into account microbial trophic steps. Trophic position, but not the relative importance of the microbial food web, increased with individual size, suggesting that current estimates of the trophic position of top consumers and of the length of oceanic food webs are too low because they are based only on metazoan trophic steps. This finding calls for a review of trophic position estimates and of the efficiency of trophic transfers along oceanic food webs.

Amino acid δ15N underestimation of cetacean trophic positions highlights limited understanding of isotopic fractionation in higher marine consumers.

Compound‐specific stable isotope analysis (CSIA) of amino acids (AAs) has been rapidly incorporated in ecological studies to resolve consumer trophic position (TP). Differential 15N fractionation of “trophic” AAs, which undergo trophic 15N enrichment, and “source” AAs, which undergo minimal trophic 15N enrichment and serve as a proxy for primary producer δ15N values, allows for internal calibration of TP. Recent studies, however, have shown the difference between source and trophic AA δ15N values in higher marine consumers is less than predicted from empirical studies of invertebrates and fish. To evaluate CSIA‐AA for estimating TP of cetaceans, we compared source and trophic AA δ15N values of multiple tissues (skin, baleen, and dentine collagen) from five species representing a range of TPs: bowhead whales, beluga whales, short‐beaked common dolphins, sperm whales, and fish‐eating (FE) and marine mammal‐eating (MME) killer whale ecotypes. TP estimates (TPCSIA) using several empirically derived equations and trophic discrimination factors (TDFs) were 1–2.5 trophic steps lower than stomach content‐derived estimates (TPSC) for all species. Although TPCSIA estimates using dual TDF equations were in better agreement with TPSC estimates, our data do not support the application of universal or currently available dual TDFs to estimate cetacean TPs. Discrepancies were not simply due to inaccurate TDFs, however, because the difference between consumer glutamic acid/glutamine (Glx) and phenylalanine (Phe) δ15N values (δ15NGlx‐Phe) did not follow expected TP order. In contrast to pioneering studies on invertebrates and fish, our data suggest trophic 15N enrichment of Phe is not negligible and should be examined among the potential mechanisms driving “compressed” and variable δ15NGlx‐Phe values at high TPs. We emphasize the need for controlled diet studies to understand mechanisms driving AA‐specific isotopic fractionation before widespread application of CSIA‐AA in ecological studies of cetaceans and other marine consumers.

A multi-isotope analysis of Neolithic human groups in the Yonne valley, Northern France: insights into dietary patterns and social structure

With the arrival of the Neolithic to Europe, new ways of life and new subsistence strategies emerged. In the Paris Basin (northern France), the appearance of some monumental funerary structures during the Middle Neolithic highlights in particular the increasing complexity of the social organisation. At the same time, several sites, such as open-air cemeteries, do not display any evidence of such arrangement. In the southeast of this area, the two primary routes of neolithisation meet. Several funerary parameters attest to the diverse influence received from other surrounding cultures. In order to assess potential differences in diet, and therefore on purported social distinctions at the inter- and intra-site level, stable isotope analyses (carbon, nitrogen and sulphur) were performed on bone collagen of humans (n = 177) and non-human animals (n = 62) from seven archaeological sites located in the same area (< 10 km). This study is the biggest so far on French Neolithic material and thus allows for an extensive investigation at a regional scale. Results show that the human nitrogen isotopic ratios are relatively enriched in nitrogen-15 comparing to those of the domesticated animals. This reflects a trophic step that is rarely observed elsewhere in the surrounding Neolithic people, particularly for humans of the biggest site Gurgy “Les Noisats”. Though zooarchaeological data support a predominant cattle consumption, here, we propose a mixed protein consumption of cattle and pig, possibly complemented with some freshwater resources. Furthermore, carbon, nitrogen and sulphur isotopic ratios suggest some slight differences between sexes and sites. This sexual distinction has rarely been identified in the diet within a Neolithic context. Some variations over time were also detected. On the whole, this study seems to support previous observations made from burial practices about a specific regional Neolithic pattern in the Paris Basin as well as bring new elements into discussion of social organisation in human populations.

Calcium isotopes in enamel of modern and Plio-Pleistocene East African mammals

Calcium isotope analyses show a depletion of heavy calcium isotopes in vertebrates, compared to food sources along each trophic step. Recent studies show considerable variability of the calcium isotopic composition of bone and teeth in modern mammals, leading to inconclusive interpretations regarding the utility of Ca isotopes for trophic inference in mammal-dominated terrestrial ecosystems. Here, we analyzed modern enamel samples from the Tsavo National Park (Kenya), and fossil enamel samples dated from ca. 4 Ma to 1.6 Ma from the Turkana Basin (Kenya). We found a constancy of taxa ordering between the modern and fossil datasets, suggesting that the diagenesis of calcium isotopes is minimal in fossils. In modern herbivore samples using similar digestive physiologies, browsers are enriched in 44Ca compared to grazers. Both grazer and browser herbivore tooth enamel is enriched in 44Ca relative to carnivores by about +0.30‰. Used together, carbon and calcium isotope compositions may help refine the structure of the C3 and C4 trophic chains in the fossil record. Due to their high preservation potential, combining both carbon and calcium isotope systems represent a reliable approach to the reconstruction of the structure of past ecosystems.

Feeding strategies for the acquisition of high-quality food sources in stream macroinvertebrates: Collecting, integrating, and mixed feeding.

Aquatic macroinvertebrates play an important functional role in energy transfer in food webs, linking basal food sources to upper trophic levels that include fish, birds, and humans. However, the trophic coupling of nutritional quality between macroinvertebrates and their food sources is still poorly understood. We conducted a field study in subalpine streams in Austria to investigate how the nutritional quality (measured by long‐chain polyunsaturated fatty acids, LC‐PUFAs) in macroinvertebrates changes relative to their basal food sources. Samples of macroinvertebrates, periphyton, and leaves were collected from 17 streams in July and October 2016 and their fatty acid (FA) composition was analyzed. Periphyton FA varied strongly with time and space, and their trophic effect on macroinvertebrate FA differed among functional feeding groups. The match between periphyton FA and macroinvertebrate FA decreased with increasing trophic levels, but LC‐PUFA content increased with each trophic step from periphyton to grazers and finally predators. Macroinvertebrates fed selectively on, assimilated, and/or actively controlled their LC‐PUFA, especially eicosapentaenoic acid (EPA, 20 : 5ω3) relative to their basal food sources in the face of spatial and temporal changes. Grazer FA profiles reflected periphyton FA with relatively good fidelity, and especially their EPA feeding strategy was primarily linked to periphyton FA variation across seasons. In contrast, shredders appeared to preferentially assimilate more EPA over other FA, which was determined by the availability of high‐quality food over seasons. Predators may more actively control their LC‐PUFA distribution with respect to different quality foods and showed less fidelity to the basal FA profiles in plants and prey. Overall, grazers and shredders showed relatively good fidelity to food FA profiles and performed as both “collectors” and “integrators” for LC‐PUFA requirements across seasons, while predators at higher trophic levels were more “integrators” with added metabolic complexity leading to somewhat more divergent FA profiles. These results are potentially applicable for other aquatic consumers in freshwater and marine ecosystems.

Trophic ecology of barrelfish (Hyperoglyphe perciformis) in oceanic waters of southeast Florida

Deep-water demersal fishes represent an understudied but ecologically important group of organisms. Select species of demersal fishes rely on pelagic prey items, representing a direct transport of surface carbon to greater depths. Barrelfish,Hyperoglyphe perciformis (Mitchell, 1818), which inhabit deep slope waters, are a species that has been suggested to fill this role, as congeners consume primarily pelagic gelatinous zooplankton. However, there is a dearth of information on the trophic ecology of barrelfish. Stomach content and stable isotope analyses were conducted on 29 barrelfish caught by recreational fishers from November 2014 to November 2015 off Miami, Florida, to improve our understanding of the feeding of this species.Pyrosoma atlanticum Peron, 1804, a pelagic, vertically migrating tunicate, represented 89% of the barrelfish diet by weight. Mesopelagic fish and shrimp contributed much smaller proportions. Standard ellipse areas corrected for sample size (SEAc ) showed a substantially smaller isotopic niche width for barrelfish (n = 26, 0.606 ‰2) than dolphinfish, Coryphaena hippurus Linnaeus, 1758 (n = 36, 2.16 ‰2), king mackerel,Scomberomorus cavalla (Cuvier, 1829) (n = 17, 3.04 ‰2), or wahoo,Acanthocybium solandri (Cuvier, 1832) (n = 12, 1.97 ‰2). Coupled with dependence on a singular prey item, the low SEAc of barrelfish suggests they occupy a limited trophic niche space. Overlap of barrelfish SEAc with dolphinfish (99.5% overlap) and king mackerel (100% overlap) indicate that the carbon sources and the number of trophic steps for barrelfish are similar to king mackerel and dolphinfish, and are linked to surface waters. This trophic linkage suggests that barrelfish may play a role in carbon export and further study of their behavior and daily consumption rates is warranted for quantifying this role.

Protistan microzooplankton and the trophic position of tuna: quantifying the trophic link between micro- and mesozooplankton in marine foodwebs

Abstract The importance of the trophic link between &amp;lt;200-µm protistan microzooplankton and mesozooplankton is a cornerstone of modern understanding of foodweb structure of marine pelagic ecosystems that is well demonstrated in experimentally measured contributions of protistan consumers to mesozooplankton diets, in constrained global budgets, and in regional studies that show the inadequacies of meeting zooplankton metabolic requirements by herbivory alone. Nonetheless, protistan trophic steps are poorly reflected in stable isotope analyses by standard methods and systematically neglected in fisheries-related trophic research, which focuses instead on interactions that can be measured in stomach contents. Here, we apply recent advances in compound-specific isotope analysis of amino acids (CSIA-AA) based on alanine as a trophic indicator of protistan foodweb steps to evaluate the implications of lower foodweb structure on trophic position (TP) estimates of tunas. CSIA-AA results for mesozooplankton of the subtropical North Pacific suggest that tuna TPs are underestimated by 0.9, which give rise to new TP estimates of 4.7–5.4 for the three main tuna species of that region. These, in turn, are used to compute a trophic enrichment factor (TEF = 4.45) based on alanine that includes 15N enrichments for protistan consumers and can be applied more broadly in the region. Accounting for the magnitude and variability of protistan trophic steps in the foodwebs supporting pelagic fisheries has important implications for understanding regional variability in energy flows and foodweb structure and their temporal responses to climate change.

Seasonal variation in stable carbon and nitrogen isotope values of bats reflect environmental baselines.

The stable carbon and nitrogen isotope composition of animal tissues is commonly used to trace wildlife diets and analyze food chains. Changes in an animal’s isotopic values over time are generally assumed to indicate diet shifts or, less frequently, physiological changes. Although plant isotopic values are known to correlate with climatic seasonality, only a few studies restricted to aquatic environments have investigated whether temporal isotopic varia-tion in consumers may also reflect environmental baselines through trophic propagation. We modeled the monthly variation in carbon and nitrogen isotope values in whole blood of four insectivorous bat species occupying different foraging niches in southern Spain. We found a common pattern of isotopic variation independent of feeding habits, with an overall change as large as or larger than one trophic step. Physiological changes related to reproduction or to fat deposition prior to hibernation had no effect on isotopic variation, but juvenile bats had higher δ13C and δ15N values than adults. Aridity was the factor that best explained isotopic variation: bat blood became enriched in both 13C and 15N after hotter and/or drier periods. Our study is the first to show that consumers in terrestrial ecosystems reflect seasonal environmental dynamics in their isotope values. We highlight the danger of misinterpreting stable isotope data when not accounting for seasonal isotopic baselines in food web studies. Understanding how environmental seasonality is inte-grated in animals’ isotope values will be crucial for developing reliable methods to use stable isotopes as dietary tracers.

Isotopic invisibility of protozoan trophic steps in marine food webs

According to modern oceanographic perspectives that emphasize microbial pathways, phagotrophic protists comprise one to several levels of intermediate consumers between phytoplankton and larger metazooplankton (copepods and krill). However, recent attempts to quantify pelagic trophic structure in the open ocean using nitrogen stable isotope techniques have brought into question whether such measurements adequately account for protistan trophic steps. Here, we use a two‐stage chemostat system, with Dunaliella tertiolecta and Oxyrrhis marina as a predator—prey model, to address this question experimentally. To investigate 15N trophic discrimination under different conditions of nitrogen availability and recycling, Oxyrrhis was fed in the light and in the dark on phytoplankton provided with high and low nutrient ratios of N : P. We used both bulk and amino acids—compound specific isotopic analysis (AA—CSIA) to distinguish trophic fractionation from changes in the δ15N values of phytoplankton (isotopic baseline). Results demonstrate that protistan consumers are not, in fact, significantly enriched in 15N relative to their prey, a marked departure from the general findings for metazoan consumers. In addition, we show that changes in the isotopic baseline propagate rapidly through the protistan food chain, highlighting the need to account for this variability at ecologically relevant time scales. If protistan trophic steps are largely invisible or significantly underestimated using nitrogen isotope measurements, research that utilize such measurements in ecological, fisheries, and climate change studies may miss a large part of the ocean's variability in food‐web structure and ecosystem function.

Amino acid 15N trophic enrichment factors of four large carnivorous fishes

Ecosystem-based fisheries management strategies require knowledge of trophic relationships. Trophic position (TP) estimates from compound specific nitrogen isotopic analysis of amino acids (AA-CSIA) show promise as the method can disentangle confounding factors associated with changing δ15N values at the base of the food web, but it has yet to be tested in many organisms. This novel technique requires two empirically determined biological parameters: 1) β, the difference in δ15N values between glutamic acid (glu) and phenylalanine (phe) in primary producers and 2) trophic enrichment factor (TEF), the 15N enrichment of glu and phe at each trophic step. Values of β (3.4‰) and TEF (7.6‰) have been suggested for animals in aquatic environments; however recent observations indicate that TEF values may be variable, particularly among elasmobranchs where urea retention may alter nitrogen isotope fractionation between glu and phe. To test these uncertainties, we determined TEF values for three species of sharks, sand tiger (Carcharias taurus), lemon (Negaprion brevirostris), and leopard sharks (Triakis semifasciata), and one teleost species, opakapaka (Pristipomoides filamentosus) grown on controlled and well characterized diets for durations ranging from three (T. semifasciata) to over five years (P. filamentosus). TEF values for both elasmobranchs and opakapaka were ~2‰, significantly lower than TEFs previously reported. These results do not support the hypothesis that urea retention lowers 15N trophic enrichment between glu and phe in elasmobranchs. Rather, isotopic enrichment factors may be primarily driven by differences in dietary protein quality, leading to distinct TEFs for herbivores (~7.6‰) and carnivores (<7.6‰). We propose a method to calculate TP which integrates different TEF values for herbivores and carnivores.