Resource partitioning of a Mexican clam in species-poor Baltic Sea sediments indicates the existence of a vacant trophic niche.

Invasive species are often generalists that can take advantage of formerly unexploited resources. The existence of such vacant niches is more likely in species-poor systems like the Baltic Sea. The suspension feeding wedge clam, Rangia cuneata, native to estuarine environments in the Gulf of Mexico, was sighted for the first time in the southeastern Baltic in 2010 and a few years later in the northern Baltic along the Swedish coast. To explore possible competition for food resources between R. cuneata and the three native clams inhabiting Baltic shallow soft bottoms, stable isotope and fatty acid analyses were conducted. There was no overlap between R. cuneata and any of the native species in either stable isotope or fatty acid niches. This suggests efficient partitioning of resources; multivariate analyses indicate that separation was driven mainly by δ13C and by fatty acids reflecting diatoms and cyanobacteria, respectively (e.g. 16:1ω7 and 18:3ω3). R. cuneata reflected seasonal variation in phytoplankton more than other clams reflecting higher trophic plasticity. In conclusion, the addition of R. cuneata to the Baltic shallow soft bottoms suggests the existence of a vacant trophic niche in these sediment habitats, however the long-term effects on other species and nutrient cycling requires further studies focusing on the population dynamics of R. cuneata and its impact on the Baltic Sea ecosystem.

High capacity for a dietary specialist consumer population to cope with increasing cyanobacterial blooms.

We present a common-garden experiment to examine the amphipod Monoporeia affinis, a key deposit-feeder in the Baltic Sea, a low diversity system offering a good model for studying local adaptations. In the northern part of this system, the seasonal development of phytoplankton is characterized by a single diatom bloom (high nutritional quality), whereas in the south, the diatom bloom is followed by a cyanobacteria bloom (low nutritional quality) during summer. Therefore, the nutrient input to the benthic system differs between the sea basins. Accordingly, the amphipod populations were expected to be dietary specialists in the north and generalists in the south. We tested this hypothesis using a combination of stable isotope tracers, trophic niche analyses, and various endpoints of growth and health status. We found that when mixed with diatomes, the toxin-producing cyanobacteria, were efficiently incorporated and used for growth by both populations. However, contrary to expectations, the feeding plasticity was more pronounced in the northern population, indicating genetically-based divergence and suggesting that these animals can develop ecological adaptations to the climate-induced northward cyanobacteria expansion in this system. These findings improve our understanding regarding possible adaptations of the deposit-feeders to increasing cyanobacteria under global warming world in both limnic and marine ecosystems. It is possible that the observed effects apply to other consumers facing altered food quality due to environmental changes.

Correlating seasonal changes of naturally produced brominated compounds to biomarkers in perch from the Baltic Sea.

Hydroxylated polybrominated diphenyl ethers (OH-PBDEs), naturally produced by algae and cyanobacteria in the Baltic Sea, are potent disrupters of energy metabolism as well as endocrine disruptors and neurotoxins. In this study, European perch (Perca fluviatilis) from the Baltic Sea were sampled from May until October. OH-PBDEs and ten biomarkers were measured in each individual (n = 84 over 18 sampling time points) to study potential correlations between exposure to OH-PBDEs and changes in biomarkers. Several biomarkers showed significant non-linear seasonal variation. In the perch, ethoxyresorufin-O-deethylase (EROD) activity, plasma lactate concentration, and plasma glucose concentration showed a significant positive log-linear correlation with OH-PBDEs, whereas lipid percentage and liver somatic index showed a significant negative log-linear correlation with OH-PBDEs. These results strengthen the concern that OH-PBDEs could cause negative health effects for fish in the Baltic Sea.

Polycyclic aromatic hydrocarbons and stable isotopes of carbon and nitrogen in Baltic Sea blue mussels: Time series data 1981-2016.

Blue mussels are a target species in contaminant monitoring regarding Polycyclic Aromatic Hydrocarbons (PAHs) in biota, and also used as an isotope baseline for trophic position assessment in other biota. The latter is crucial for calculating biomagnification potential of environmental contaminants. This data set comprises long-term time series of PAHs (15 individual substances) in Baltic Sea blue mussels (Mytilus trossulus edulis) from Kvädöfjärden (collected from a depth of 5-10 m), a reference area along the Swedish coast in the Baltic Proper from 25 years during 1987-2016, and of stable isotopes in five individuals (2 cm mussels) per year during the time period 1981-2017. The data has been co-analysed with environmental (oceanographic) data in "The importance of adjusting contaminant concentrations using environmental data: a retrospective study of 25 years data in Baltic blue mussels" published in: Science of the Total Environment (https://doi.org/10.1016/j.scitotenv.2020.143913).

The importance of adjusting contaminant concentrations using environmental data: A retrospective study of 25 years data in Baltic blue mussels.

To improve the statistical power of detecting changes in contaminant concentrations over time, it is critical to reduce both the within- and between-year variability by adjusting the data for relevant confounding variables. In this study, we present a method for handling multiple confounding variables in contaminant monitoring. We evaluate the highly variable temporal trends of Polycyclic Aromatic Hydrocarbons (PAHs) in blue mussels from the central Baltic Sea during the period 1987-2016 (data from 25 years during this period) using various regression analyses. As potential explanatory variables related to PAH exposure, we use mussel size and retrospective analyses of mussel δ15N and δ13C (representing large scale biogeochemical changes as a result of e.g. eutrophication and terrestrial inputs). Environmental data from concurrent monitoring programmes (seasonal data on Chlorophyll-a, salinity and temperature in the water column, bioturbation of sediment dwelling fauna) were included as variables related to feeding conditions. The concentrations of high-molecular-weight and low-molecular-weight PAHs in blue mussel were statistically linked to different combinations of environmental variables. Adjustment using these predictors decreased the coefficient of variation in all 15 PAHs tested and improved the statistical power to detect changes. Moreover, the adjustment also resulted in a significant downward trend for fluoranthene that could not be detected initially. For another PAH, benzo(g,h,i)perylene, adjustment which reduced variation resulted in the loss of an apparent downward trend over time. Hence, our study highlights the importance of using auxilliary data to reduce variability caused by environmental factors with general effects on physiology when assessing contaminant time trends. Furthermore, it illustrates the importance of extensive and well designed monitoring programmes to provide relevant data.

Nitrogen isotope composition of amino acids reveals trophic partitioning in two sympatric amphipods.

According to ecological theory, two species cannot occupy the same niche. Using nitrogen isotope analyses (δ15N) of amino acids, we tested the extent to which two sympatric deposit-feeding amphipods, Monoporeia affinis and Pontoporeia femorata, partition their trophic resources. We found that trophic position (TP) and resynthesis index (∑V; a proxy for degradation status of ingested material prior to assimilation by the consumer) differ between species. The surface-feeding M. affinis had higher TP and intermediate ∑V, both pointing to a large contribution of metazoans in its diet. P. femorata, which feeds in the subsurface layers, had lower TP and a bimodal distribution of the ∑V values, supporting previous experimental evidence of a larger feeding niche. We also evaluated whether TP and ∑V values have consequences for amphipod fecundity and embryo viability and found that embryo viability in M. affinis was negatively linked to TP. Our results indicate that the amino acid-δ15N data paired with information about reproductive status are useful for detecting differences in the trophic ecology of sympatric amphipods.

Ecological changes as a plausible explanation for differences in uptake of contaminants between European perch and eelpout in a coastal area of the Baltic Sea.

Unexpected increasing trends in the concentration of contaminants in European perch (Perca fluviatilis) and in activity of ethoxyresorufin-O-deethylase (EROD) in European perch and eelpout (Zoarces viviparus) have been observed at a Swedish coastal reference site. This study uses data from different sources to investigate plausible explanations. The results showed that a change in diet and an improved overall condition coincide with an increase in mercury in European perch. Furthermore, an increase in several organic contaminants in European perch coincided with the introduction of an invasive deep-burrowing polychaete, which likely contributed to the release of contaminants through bioturbation. The increase in EROD-activity in both species seems to be related to contaminants that reach the fish through the water rather than the diet. The results show that for contaminants that are taken up via the diet, trends in contamination can be opposite for different species of fish in the same area.

Linking consumer physiological status to food-web structure and prey food value in the Baltic Sea.

Declining physiological status in marine top consumers has been observed worldwide. We investigate changes in the physiological status and population/community traits of six consumer species/groups in the Baltic Sea (1993-2014), spanning four trophic levels and using metrics currently operational or proposed as indicators of food-web status. We ask whether the physiological status of consumers can be explained by food-web structure and prey food value. This was tested using partial least square regressions with status metrics for gray seal, cod, herring, sprat and the benthic predatory isopod Saduria as response variables, and abundance and food value of their prey, abundance of competitors and predators as predictors. We find evidence that the physiological status of cod, herring and sprat is influenced by competition, predation, and prey availability; herring and sprat status also by prey size. Our study highlights the need for management approaches that account for species interactions across multiple trophic levels.

Insufficient evidence for BMAA transfer in the pelagic and benthic food webs in the Baltic Sea.

The evidence regarding BMAA occurrence in the Baltic Sea is contradictory, with benthic sources appearing to be more important than pelagic ones. The latter is counterintuitive considering that the identified sources of this compound in the food webs are pelagic primary producers, such as diatoms, dinoflagellates, and cyanobacteria. To elucidate BMAA distribution, we analyzed BMAA in the pelagic and benthic food webs in the Northern Baltic Proper. As potential sources, phytoplankton communities were used. Pelagic food chain was represented by zooplankton, mysids and zooplanktivorous fish, whereas benthic invertebrates and benthivorous fish comprised the benthic chain. The trophic structure of the system was confirmed by stable isotope analysis. Contrary to the reported ubiquitous occurrence of BMAA in the Baltic food webs, only phytoplankton, zooplankton and mysids tested positive, whereas no measurable levels of this compound occurred in the benthic invertebrates and any of the tested fish species. These findings do not support the widely assumed occurrence and transfer of BMAA to the top consumers in the Baltic food webs. More controlled experiments and field observations are needed to understand the transfer and possible transformation of BMAA in the food web under various environmental settings.

Isotopic niche reflects stress-induced variability in physiological status.

The isotopic niche has become an established concept in trophic ecology. However, the assumptions behind this approach have rarely been evaluated. Evidence is accumulating that physiological stress can affect both magnitude and inter-individual variability of the isotopic signature in consumers via alterations in metabolic pathways. We hypothesized that stress factors (inadequate nutrition, parasite infestations, and exposure to toxic substances or varying oxygen conditions) might lead to suboptimal physiological performance and altered stable isotope signatures. The latter can be misinterpreted as alterations in isotopic niche. This hypothesis was tested by inducing physiological stress in the deposit-feeding amphipod Monoporeia affinis exposed to either different feeding regimes or contaminated sediments. In the amphipods, we measured body condition indices or reproductive output to assess growth status and δ13C and δ15N values to derive isotope niche metrics. As hypothesized, greater isotopic niche estimates were derived for the stressed animals compared to the control groups. Moreover, the δ15N values were influenced by body size, reproductive status and parasite infestations, while δ13C values were influenced by body size, oxygen conditions and survival. Using regression analysis with isotope composition and growth variables as predictors, we were able to discriminate between the amphipods exposed to nutritionally or chemically stressful conditions and those in the control groups. Thus, interpretation of isotopic niche can be confounded by natural or anthropogenic stressors that may induce an apparent change in isotopic niche. These findings stress the importance of including measures of growth and health status when evaluating stable isotope data in food web studies.

Using Compound-Specific and Bulk Stable Isotope Analysis for Trophic Positioning of Bivalves in Contaminated Baltic Sea Sediments.

Stable nitrogen isotopes (δ15N) are used as indicators of trophic position (TP) of consumers. Deriving TP from δ15N of individual amino acids (AAs) is becoming popular in ecological studies, because of lower uncertainty than TP based on bulk δ15N (TPbulk). This method would also facilitate biomagnification studies provided that isotope fractionation is unaffected by toxic exposure. We compared TPAA and TPbulk estimates for a sediment-dwelling bivalve from two coastal sites, a pristine and a contaminated. Chemical analysis of PCB levels in mussels, sediments, and pore water confirmed the expected difference between sites. Both methods, but in particular the TPAA underestimated the actual TP of bivalves. Using error propagation, the total uncertainty related to the analytical precision and assumptions in the TP calculations was found to be similar between the two methods. Interestingly, the significantly higher intercept for the regression between TPAA and TPbulk in the contaminated site compared to the pristine site indicates a higher deamination rate due to detoxification as a result of chronic exposure and a higher 15N fractionation. Hence, there is a need for controlled experiments on assumptions underlying amino acid-specific stable isotope methods in food web and bimagnification studies.

Density of Key-Species Determines Efficiency of Macroalgae Detritus Uptake by Intertidal Benthic Communities.

Accumulating evidence shows that increased biodiversity has a positive effect on ecosystem functioning, but the mechanisms that underpin this positive relationship are contentious. Complete extinctions of regional species pools are comparatively rare whereas compositional changes and reductions in abundance and biomass are common, although seldom the focus of biodiversity-ecosystem functioning studies. We use natural, small-scale patchiness in the density of two species of large bivalves with contrasting feeding modes (the suspension-feeding Austrovenus stutchburyi and deposit-feeding Macomona liliana) to examine their influence on the uptake of nitrogen from macroalgae detritus (i.e. measure of ecosystem function and food web efficiency) by other infauna in a 10-d laboratory isotope-tracer experiment. We predicted that densities of these key bivalve species and functional group diversity (calculated as Shannons H, a density-independent measure of community composition) of the intact infaunal community will be critical factors explaining variance in macroalgal per capita uptake rates by the community members and hence determine total uptake by the community. Results show that only two species, M. liliana and a large orbiniid polychaete (Scoloplos cylindrifer) dominated macroalgal nitrogen taken up by the whole community due to their large biomass. However, their densities were mostly not important or negatively influenced per capita uptake by other species. Instead, the density of a head-down deposit-feeder (the capitellid Heteromastus filiformis), scavengers (mainly nemertines and nereids) and species and functional group diversity, best explained per capita uptake rates in community members. Our results demonstrate the importance of species identity, density and large body size for ecosystem functioning and highlight the complex interactions underlying loss of ecological functions with declining biodiversity and compositional changes.

Nitrogen fixation by cyanobacteria stimulates production in Baltic food webs.

Filamentous, nitrogen-fixing cyanobacteria form extensive summer blooms in the Baltic Sea. Their ability to fix dissolved N2 allows cyanobacteria to circumvent the general summer nitrogen limitation, while also generating a supply of novel bioavailable nitrogen for the food web. However, the fate of the nitrogen fixed by cyanobacteria remains unresolved, as does its importance for secondary production in the Baltic Sea. Here, we synthesize recent experimental and field studies providing strong empirical evidence that cyanobacterial nitrogen is efficiently assimilated and transferred in Baltic food webs via two major pathways: directly by grazing on fresh or decaying cyanobacteria and indirectly through the uptake by other phytoplankton and microbes of bioavailable nitrogen exuded from cyanobacterial cells. This information is an essential step toward guiding nutrient management to minimize noxious blooms without overly reducing secondary production, and ultimately most probably fish production in the Baltic Sea.

Do deposit-feeders compete? Isotopic niche analysis of an invasion in a species-poor system.

Successful establishment of invasive species is often related to the existence of vacant niches. Competition occurs when invaders use the same limiting resources as members of the recipient community, which will be reflected in some overlap of their trophic niches. The concept of isotopic niche has been used to study trophic niche partitioning among species. Here, we present a two-year field study comparing isotopic niches of the deposit-feeding community in a naturally species-poor system. The isotopic niche analyses showed no overlap between a recent polychaete invader and any of the native species suggesting that it has occupied a vacant niche. Its narrow isotopic niche suggests specialized feeding, however, the high δ(15)N values compared to natives are most likely due to isotope fractionation effects related to nitrogen recycling and a mismatch between biological stoichiometry of the polychaete and the sediment nitrogen content. Notably, highly overlapping isotopic niches were inferred for the native species, which is surprising in a food-limited system. Therefore, our results demonstrate that invaders may broaden the community trophic diversity and enhance resource utilization, but also raise questions about the congruence between trophic and isotopic niche concepts and call for careful examination of assumptions underlying isotopic niche interpretation.

Stable isotope composition in Daphnia is modulated by growth, temperature, and toxic exposure: implications for trophic magnification factor assessment.

The potential for using stable isotope analysis in risk assessment of environmental contaminants is crucially dependent on the predictability of the trophic transfer of isotopes in food webs. The relationship between contaminant levels and trophic position of consumers is widely used to assess biomagnification properties of various pollutants by establishing trophic magnification factors (TMF). However, contaminant-induced variability of the isotopic composition in biota is poorly understood. Here, we investigated effects of toxic exposure on δ(15)N and δ(13)C values in a consumer, with a main hypothesis that these effects would be largely mediated via growth rate and metabolic turnover of the test animals. The cladoceran Daphnia magna was used in two experiments that were conducted to manipulate growth and body condition (assayed as C:N ratio) by food availability and temperature (Experiment 1) and by toxic exposure to the pesticide lindane (Experiment 2). We found a significant negative effect of growth rate and a positive effect of temperature on the consumer-diet discrimination factor for δ(15)N and δ(13)C, with no effects on the C:N ratio (Experiment 1). In lindane-exposed daphnids, a significant growth inhibition was observed, with concomitant increase in metabolic costs and significantly elevated size-specific δ(15)N and δ(13)C values. Moreover, a significantly higher incorporation of carbon relative to nitrogen, yet a concomitant decrease in C:N ratio was observed in the exposed animals. Together, these results have methodological implications for determining trophic positions and TMF in polluted environments, where elevated δ(15)N values would translate into overestimated trophic positions and underestimated TMF. Furthermore, altered δ(13)C values may lead to erroneous food-chain assignment of the consumer in question.

Nitrogen fixed by cyanobacteria is utilized by deposit-feeders.

Benthic communities below the photic zone depend for food on allochthonous organic matter derived from seasonal phytoplankton blooms. In the Baltic Sea, the spring diatom bloom is considered the most important input of organic matter, whereas the contribution of the summer bloom dominated by diazotrophic cyanobacteria is less understood. The possible increase in cyanobacteria blooms as a consequence of eutrophication and climate change calls for evaluation of cyanobacteria effects on benthic community functioning and productivity. Here, we examine utilization of cyanobacterial nitrogen by deposit-feeding benthic macrofauna following a cyanobacteria bloom at three stations during two consecutive years and link these changes to isotopic niche and variations in body condition (assayed as C:N ratio) of the animals. Since nitrogen-fixing cyanobacteria have δ(15)N close to -2‰, we expected the δ(15)N in the deposit-feeders to decrease after the bloom if their assimilation of cyanobacteria-derived nitrogen was substantial. We also expected the settled cyanobacteria with their associated microheterotrophic community and relatively high nitrogen content to increase the isotopic niche area, trophic diversity and dietary divergence between individuals (estimated as the nearest neighbour distance) in the benthic fauna after the bloom. The three surface-feeding species (Monoporeia affinis, Macoma balthica and Marenzelleria arctia) showed significantly lower δ(15)N values after the bloom, while the sub-surface feeder Pontoporeia femorata did not. The effect of the bloom on isotopic niche varied greatly between stations; populations which increased niche area after the bloom had better body condition than populations with reduced niche, regardless of species. Thus, cyanobacterial nitrogen is efficiently integrated into the benthic food webs in the Baltic, with likely consequences for their functioning, secondary production, transfer efficiency, trophic interactions, and intra- and interspecific competition.

Polychaete invader enhances resource utilization in a species-poor system.

Ecosystem consequences of biodiversity change are often studied from a species loss perspective, while the effects of invasive species on ecosystem functions are rarely quantified. In this experimental study, we used isotope tracers to measure the incorporation and burial of carbon and nitrogen from a simulated spring phytoplankton bloom by communities of one to four species of deposit-feeding macrofauna found in the species-poor Baltic Sea. The recently invading polychaete Marenzelleria arctia, which has spread throughout the Baltic Sea, grows more rapidly than the native species Monoporeia affinis, Pontoporeia femorata (both amphipods) and Macoma balthica (a bivalve), resulting in higher biomass increase (biomass production) in treatments including the polychaete. Marenzelleria incorporated and buried bloom material at rates similar to the native species. Multi-species treatments generally had higher isotope incorporation, indicative of utilization of bloom material, than expected from monoculture yields of the respective species. The mechanism behind this observed over-yielding was mainly niche complementarity in utilization of the bloom input, and was more evident in communities including the invader. In contrast, multi-species treatments had generally lower biomass increase than expected. This contrasting pattern suggests that there is little overlap in resource use of freshly deposited bloom material between Marenzelleria and the native species but it is likely that interference competition acts to dampen resulting community biomass. In conclusion, an invasive species can enhance incorporation and burial of organic matter from settled phytoplankton blooms, two processes fundamental for marine productivity.

Diversity of larger consumers enhances interference competition effects on smaller competitors.

Competition between large and small species for the same food is common in a number of ecosystems including aquatic ones. How diversity of larger consumers affects the access of smaller competitors to a limiting resource is not well understood. We tested experimentally how species richness (0-3 spp.) of benthic deposit-feeding macrofauna changes meiofaunal ostracods' incorporation of fresh organic matter from a stable-isotope-labeled cyanobacterial bloom, using fauna from the species-poor Baltic Sea. Presence of macrofauna mostly decreased meiofaunal incorporation of bloom material, depending on the macrofauna species present. As expected, the species identity of macrofauna influenced the incorporation of organic matter by meiofauna. Interestingly, our results show that, in addition, species richness of the macrofauna significantly reduced meiofauna incorporation of freshly settled nitrogen and carbon. With more than one macrofauna species, the reduction was always greater than expected from the single-species treatments. Field data from the Baltic Sea showed a negative correlation between macrofauna diversity and meiofaunal ostracod abundance, as expected from the experimental results. We argue that this is caused by interference competition, due to spatial niche differentiation between macrofauna species reducing the sediment volume in which ostracods can feed undisturbed by larger competitors. Interference from macrofauna significantly reduces organic matter incorporation by meiofauna, indicating that diversity of larger consumers is an important factor controlling the access of smaller competitors to a limiting food resource.

Higher diversity of deposit-feeding macrofauna enhances phytodetritus processing.

The link between biodiversity and ecosystem functioning is an important question that remains unresolved, particularly in marine systems, in which cycling of organic matter by benthic organisms is of global significance. Direct observations of specific resource use by each species in single- and multispecies communities, as quantified by stable isotopes, facilitates a mechanistic understanding of the importance of each species for ecosystem functioning. We tested the effects of altered biodiversity (species richness) of deposit-feeding macrofauna on incorporation and burial of phytodetritus in combinations of three species representing natural communities found in the sediments of the species-poor Baltic Sea. The three species, two amphipods and a bivalve, had different rates of incorporation and burial and different needs for carbon (C) and nitrogen (N). The amphipods exhibited clear resource partitioning in sympatry, as a result of vertical separation in the sediment and consequent differential use of food. Communities of several species incorporated more C and N than expected from the respective single-species treatments, due to higher incorporation by surface feeders in multispecies treatments. Community incorporation of N in the most diverse treatment even exceeded N incorporation by a single-species treatment of the best-performing species, showing transgressive over-yielding. This over-yielding was primarily due to positive complementarity in all treatments. Diverse soft bottoms are also likely to be more productive in the long run, as species-specific traits (subsurface feeding) preserve fresh phytodetritus by burying it to depths in the sediment at which the mineralization rate is low. The more diverse sediment communities showed more efficient trophic transfer of phytodetritus, a finding of general significance for understanding biological processes driving the transformation of nutrients and energy in benthic ecosystems.