ABSTRACT
AbstractRhizocephalan barnacles are parasites of crustaceans that are known for dramatic effects on hosts, including parasitic castration, feminization, molt inhibition, and the facilitation of epibiosis. Most research on rhizocephalans has focused on carcinized hosts, with relatively little research directed to shrimp hosts that may experience distinct consequences of infection. Here, we describe a high-prevalence rhizocephalan-shrimp system in which multiple host changes are associated with infection: the dock shrimp Pandalus danae infected by the rhizocephalan Sylon hippolytes. In field-collected P. danae, infection by Sylon was associated with development of female sex characters at a smaller size and greater probability of epibiosis. Standardized video observations showed that infected P. danae performed grooming activities at higher rates than uninfected shrimp, suggesting that inhibited molting rather than direct behavioral modification is a likely mechanism for higher epibiosis rates. There was no difference in the composition of grooming behavior types or in general activity between infected and uninfected shrimp. Fatty acid compositions differed with infection, but total lipid concentrations did not, suggesting that parasite-driven shifts in host resource allocation were compensated or redirected from unmeasured tissues. Our results show that Sylon alters its host's role by provisioning an epibiotic substrate and also that it influences host physiology, resulting in feminization and fatty acid shifts. This study lays the groundwork for expanding rhizocephalan-shrimp research and encourages recognition of oft-ignored roles of parasitism in ecological communities.
Subject(s)
Parasites , Thoracica , Male , Humans , Animals , Female , Host-Parasite Interactions , Feminization , Thoracica/physiology , Fatty AcidsABSTRACT
The global distribution of primary production and consumption by humans (fisheries) is well-documented, but we have no map linking the central ecological process of consumption within food webs to temperature and other ecological drivers. Using standardized assays that span 105° of latitude on four continents, we show that rates of bait consumption by generalist predators in shallow marine ecosystems are tightly linked to both temperature and the composition of consumer assemblages. Unexpectedly, rates of consumption peaked at midlatitudes (25 to 35°) in both Northern and Southern Hemispheres across both seagrass and unvegetated sediment habitats. This pattern contrasts with terrestrial systems, where biotic interactions reportedly weaken away from the equator, but it parallels an emerging pattern of a subtropical peak in marine biodiversity. The higher consumption at midlatitudes was closely related to the type of consumers present, which explained rates of consumption better than consumer density, biomass, species diversity, or habitat. Indeed, the apparent effect of temperature on consumption was mostly driven by temperature-associated turnover in consumer community composition. Our findings reinforce the key influence of climate warming on altered species composition and highlight its implications for the functioning of Earth's ecosystems.
Subject(s)
Biodiversity , Climate , Fisheries , Food Chain , Alismatales , Animals , Biomass , Female , Fishes , Geography , Global Warming , Humans , MaleABSTRACT
Determining the transfer and transformation of organic matter in food webs is a fundamental challenge that has implications for sustainable management of ecosystems. Fatty acids (FA) offer a potential approach for resolving complex diet mixtures of organisms because they provide a suite of molecular tracers. Yet, uncertainties in the degree of their biochemical modification by consumers, due to selective retention or metabolism, have limited their application. Here, we consolidated 316 controlled feeding studies of aquatic ectotherms (fishes and invertebrates) involving 1404 species-diet combinations to assess the degree of trophic modification of FA in muscle tissue. We found a high degree of variability within and among taxa in the %FA in consumer muscle tissue versus %FA in diet regression equations. Most saturated FA had weak relationships with the diet (r2 < 0.30) and shallow slopes (m < 0.30), suggesting a lack of retention in muscle when fed in increasing amounts. Contrarily, several essential FA, including linoleic (18:2n-6) and α-linolenic acid (18:3n-3), exhibited significant relationships with the diet (m > 0.35, r2 > 0.50), suggesting supply limitations and selective retention in muscle by consumers. For all FA, relationships strengthened with increasing taxonomic specificity. We also demonstrated the utility of new correction equations by calculating the potential contributions of approximately 20 prey items to the diet of selected species of generalist fishes using a FA mixing model. Our analyses further reveal how a broad range of fishes and invertebrates convert or store these compounds in muscle tissue to meet physiological needs and point to their power in resolving complex diets in aquatic food webs. This article is part of the theme issue 'The next horizons for lipids as 'trophic biomarkers': evidence and significance of consumer modification of dietary fatty acids'.
Subject(s)
Aquatic Organisms/metabolism , Biomarkers/metabolism , Fatty Acids/metabolism , Fishes/metabolism , Invertebrates/metabolism , Animals , Diet/veterinaryABSTRACT
Fatty acids are commonly used as biomarkers for making inferences about trophic relationships in aquatic and soil food webs. However, researchers are often unaware of the physiological constraints within organisms on the trophic transfer and modification of dietary biomarkers in consumers. Fatty acids are bioactive molecules, which have diverse structures and functions that both complicate and enhance their value as trophic tracers. For instance, consumers may synthesize confounding non-dietary sourced markers from precursor molecules, and environmental conditions also affect fatty acid composition. There is a vital need for more research on the uptake and transfer of trophic biomarkers in individual organisms in order to advance the field and make meaningful use of these tools at the scale of populations or ecosystems. This special issue is focused on controlled feeding experiments on a diverse taxonomic breadth of model consumers from freshwater, marine and soil ecosystems with a goal of creating a more integrated understanding of the connection between consumer physiology and trophic ecology. This article is part of the theme issue 'The next horizons for lipids as 'trophic biomarkers': evidence and significance of consumer modification of dietary fatty acids'.
Subject(s)
Biomarkers/analysis , Ecosystem , Fatty Acids/metabolism , Food Chain , Fresh Water , Seawater , SoilABSTRACT
Dungeness crabs (Metacarcinus magister) are ecologically and economically important in the coastal Northeast Pacific, yet relatively little is currently known about their feeding behaviour in the wild or their natural diet. Trophic biomarkers, such as fatty acids (FA), can be used to reveal trophic interactions. We used two feeding experiments to assess differences in FA composition of juvenile crabs fed different known foods to evaluate how they modify and integrate dietary FA into their own tissues and determine whether crab FA reflect diet changes over a six-week period. These experimental results were then compared with the FA signatures of wild caught juvenile crab with undetermined diets. We found that juvenile Dungeness crabs fed different foods assimilated dietary FA into their tissues and were distinct in their FA signatures when analysed with multivariate statistics. Experimentally fed juvenile crabs contained greater proportions of the most abundant long-chain polyunsaturated fatty acids (LCPUFA, >C20) than their foods. Crabs fed foods lacking in LCPUFA, particularly DHA (22:6ω3, docosahexaenoic acid), did not survive or grew slower than crabs fed other foods. This suggests that LCPUFA are physiologically important for this species and indicates biosynthesis of these FA does not occur or is not sufficient to meet their needs. This article is part of the theme issue 'The next horizons for lipids as 'trophic biomarkers': evidence and significance of consumer modification of dietary fatty acids'.
Subject(s)
Brachyura/chemistry , Diet , Fatty Acids/metabolism , AnimalsABSTRACT
The sea urchin Strongylocentrotus purpuratus (order Camarodonta, family Strongylocentrotidae) can be found dominating low intertidal pool biomass on the southern coast of Oregon, USA. In this case study, three adult sea urchins were collected from their shared intertidal pool, and the bacteriome of their pharynx, gut tissue, and gut digesta, including their tide pool water and algae, was determined using targeted high-throughput sequencing (HTS) of the 16S rRNA genes and bioinformatics tools. Overall, the gut tissue demonstrated Arcobacter and Sulfurimonas (Epsilonproteobacteria) to be abundant, whereas the gut digesta was dominated by Psychromonas (Gammaproteobacteria), Propionigenium (Fusobacteria), and Flavobacteriales (Bacteroidetes). Alpha and beta diversity analyses indicated low species richness and distinct microbial communities comprising the gut tissue and digesta, while the pharynx tissue had higher richness, more closely resembling the water microbiota. Predicted functional profiles showed Kyoto Encyclopedia of Genes and Genomes (KEGG) Level-2 categories of energy metabolism, membrane transport, cell motility, and signal transduction in the gut tissue, and the gut digesta represented amino acid, carbohydrate, vitamin and cofactor metabolisms, and replication and repair. Co-occurrence network analysis showed the potential relationships and key taxa, such as the highly abundant Arcobacter and Propionigenium, influencing population patterns and taxonomic organization between the gut tissue and digesta. These results demonstrate a trend of microbial community integration, allocation, predicted metabolic roles, and taxonomic co-occurrence patterns in the S. purpuratus gut ecosystem.
ABSTRACT
Winter conditions are rapidly changing in temperate ecosystems, particularly for those that experience periods of snow and ice cover. Relatively little is known of winter ecology in these systems, due to a historical research focus on summer 'growing seasons'. We executed the first global quantitative synthesis on under-ice lake ecology, including 36 abiotic and biotic variables from 42 research groups and 101 lakes, examining seasonal differences and connections as well as how seasonal differences vary with geophysical factors. Plankton were more abundant under ice than expected; mean winter values were 43.2% of summer values for chlorophyll a, 15.8% of summer phytoplankton biovolume and 25.3% of summer zooplankton density. Dissolved nitrogen concentrations were typically higher during winter, and these differences were exaggerated in smaller lakes. Lake size also influenced winter-summer patterns for dissolved organic carbon (DOC), with higher winter DOC in smaller lakes. At coarse levels of taxonomic aggregation, phytoplankton and zooplankton community composition showed few systematic differences between seasons, although literature suggests that seasonal differences are frequently lake-specific, species-specific, or occur at the level of functional group. Within the subset of lakes that had longer time series, winter influenced the subsequent summer for some nutrient variables and zooplankton biomass.
Subject(s)
Ecosystem , Ice Cover , Lakes , Plankton/physiology , SeasonsABSTRACT
Freshwater food webs can be partly supported by terrestrial primary production, often deriving from plant litter of surrounding catchment vegetation. Although consisting mainly of poorly bioavailable lignin, with low protein and lipid content, the carbohydrates from fallen tree leaves and shoreline vegetation may be utilized by aquatic consumers. Here we show that during phytoplankton deficiency, zooplankton (Daphnia magna) can benefit from terrestrial particulate organic matter by using terrestrial-origin carbohydrates for energy and sparing essential fatty acids and amino acids for somatic growth and reproduction. Assimilated terrestrial-origin fatty acids from shoreline reed particles exceeded available diet, indicating that Daphnia may convert a part of their dietary carbohydrates to saturated fatty acids. This conversion was not observed with birch leaf diets, which had lower carbohydrate content. Subsequent analysis of 21 boreal and subarctic lakes showed that diet of herbivorous zooplankton is mainly based on high-quality phytoplankton rich in essential polyunsaturated fatty acids. The proportion of low-quality diets (bacteria and terrestrial particulate organic matter) was <28% of the assimilated carbon. Taken collectively, the incorporation of terrestrial carbon into zooplankton was not directly related to the concentration of terrestrial organic matter in experiments or lakes, but rather to the low availability of phytoplankton.
Subject(s)
Daphnia/physiology , Fresh Water/chemistry , Zooplankton/physiology , Animals , Carbohydrate Metabolism , Carbohydrates , Fatty Acids/analysis , Food Chain , Lakes/chemistryABSTRACT
Essential fatty acids (EFA), which are primarily generated by phytoplankton, limit growth and reproduction in diverse heterotrophs. The biochemical composition of phytoplankton is well-known to be governed both by phylogeny and environmental conditions. Nutrients, light, salinity, and temperature all affect both phytoplankton growth and fatty acid composition. However, the relative importance of taxonomy and environment on algal fatty acid content has yet to be comparatively quantified, thus inhibiting predictions of changes to phytoplankton food quality in response to global environmental change. We compiled 1145 published marine and freshwater phytoplankton fatty acid profiles, consisting of 208 species from six major taxonomic groups, cultured in a wide range of environmental conditions, and used a multivariate distance-based linear model to quantify the total variation explained by each variable. Our results show that taxonomic group accounts for 3-4 times more variation in phytoplankton fatty acids than the most important growth condition variables. The results underscore that environmental conditions clearly affect phytoplankton fatty acid profiles, but also show that conditions account for relatively low variation compared to phylogeny. This suggests that the underlying mechanism determining basal food quality in aquatic habitats is primarily phytoplankton community composition, and allows for prediction of environmental-scale EFA dynamics based on phytoplankton community data. We used the compiled dataset to calculate seasonal dynamics of long-chain EFA (LCEFA; ≥C20 É·-3 and É·-6 polyunsaturated fatty acid) concentrations and É·-3:É·-6 EFA ratios in Lake Washington using a multi-decadal phytoplankton community time series. These analyses quantify temporal dynamics of algal-derived LCEFA and food quality in a freshwater ecosystem that has undergone large community changes as a result of shifting resource management practices, highlighting diatoms, cryptophytes and dinoflagellates as key sources of LCEFA. Moreover, the analyses indicate that future shifts towards cyanobacteria-dominated communities will result in lower LCEFA content in aquatic ecosystems.
Subject(s)
Ecosystem , Environment , Fatty Acids/metabolism , Phylogeny , Phytoplankton/growth & development , Phytoplankton/metabolism , Biomass , Phytoplankton/classificationABSTRACT
We modified the stable isotope mixing model MixSIR to infer primary producer contributions to consumer diets based on their fatty acid composition. To parameterize the algorithm, we generated a 'consumer-resource library' of FA signatures of Daphnia fed different algal diets, using 34 feeding trials representing diverse phytoplankton lineages. This library corresponds to the resource or producer file in classic Bayesian mixing models such as MixSIR or SIAR. Because this library is based on the FA profiles of zooplankton consuming known diets, and not the FA profiles of algae directly, trophic modification of consumer lipids is directly accounted for. To test the model, we simulated hypothetical Daphnia comprised of 80% diatoms, 10% green algae, and 10% cryptophytes and compared the FA signatures of these known pseudo-mixtures to outputs generated by the mixing model. The algorithm inferred these simulated consumers were comprised of 82% (63-92%) [median (2.5th to 97.5th percentile credible interval)] diatoms, 11% (4-22%) green algae, and 6% (0-25%) cryptophytes. We used the same model with published phytoplankton stable isotope (SI) data for δ13C and δ15N to examine how a SI based approach resolved a similar scenario. With SI, the algorithm inferred that the simulated consumer assimilated 52% (4-91%) diatoms, 23% (1-78%) green algae, and 18% (1-73%) cyanobacteria. The accuracy and precision of SI based estimates was extremely sensitive to both resource and consumer uncertainty, as well as the trophic fractionation assumption. These results indicate that when using only two tracers with substantial uncertainty for the putative resources, as is often the case in this class of analyses, the underdetermined constraint in consumer-resource SI analyses may be intractable. The FA based approach alleviated the underdetermined constraint because many more FA biomarkers were utilized (n < 20), different primary producers (e.g., diatoms, green algae, and cryptophytes) have very characteristic FA compositions, and the FA profiles of many aquatic primary consumers are strongly influenced by their diets.
Subject(s)
Bayes Theorem , Diet , Fatty Acids/chemistry , Food Chain , AnimalsABSTRACT
Primary productivity by plants and algae is the fundamental source of energy in virtually all food webs. Furthermore, photosynthetic organisms are the sole source for ω-3 and ω-6 essential fatty acids (EFA) to upper trophic levels. Because animals cannot synthesize EFA, these molecules may be useful as trophic markers for tracking sources of primary production through food webs if different primary producer groups have different EFA signatures. We tested the hypothesis that different marine macrophyte groups have distinct fatty acid (FA) signatures by conducting a phylogenetic survey of 40 marine macrophytes (seaweeds and seagrasses) representing 36 families, 21 orders, and four phyla in the San Juan Archipelago, WA, USA. We used multivariate statistics to show that FA composition differed significantly (P < 0.001) among phyla, orders, and families using 44 FA and a subset of seven EFA (P < 0.001). A second analysis of published EFA data of 123 additional macrophytes confirmed that this pattern was robust on a global scale (P < 0.001). This phylogenetic differentiation of macrophyte taxa shows a clear relationship between macrophyte phylogeny and FA content and strongly suggests that FA signature analyses can offer a viable approach to clarifying fundamental questions about the contribution of different basal resources to food webs. Moreover, these results imply that taxa with commercially valuable EFA signatures will likely share such characteristics with other closely related taxa that have not yet been evaluated for FA content.