Essential Biomolecules in Food Webs
- 1Ecology Group, Institute of Biology, Humboldt-Universität zu Berlin, Berlin, Germany
- 2Aquatic Ecology, University of Hamburg, Hamburg, Germany
We here review the ecological role of essential nutritional biomolecules [fatty acids (FA), amino acids (AA), sterols, vitamins] in aquatic and terrestrial food webs, encompassing the forces behind their environmental distribution. Across ecosystems, mutualistic relationships frequently ensure exchanges of vitamins between producer and demander, especially between B12 and other B vitamins as well as the AA methionine. In contrast, FA, sterols and most AA are transferred up the food chain via classical predator-prey interactions, and therefore have good biomarker potential for trophic interactions. As biomass-flow depends on the absolute amounts of potential limiting resources, considering solely the relative share in the respective biochemical group may under- or overestimate the availability to consumers. Moreover, if not accounted for, “hidden” trophic channels, such as gut symbionts as well as metabolic conversion of precursor molecules, can hamper food web analyses. Fundamental differences exist between aquatic and terrestrial ecosystems: Vitamin B12 produced by ammonium oxidizing Archaea is essential to many aquatic algae, whereas terrestrial plants escaped this dependency by using B12 independent enzymes. Long-chain ω3 polyunsaturated FA (LC-ω3PUFA) in aquatic systems mainly originate from planktonic algae, while in terrestrial systems, belowground invertebrates can well be a source, also supporting aboveground biota. Interlinks from terrestrial to aquatic ecosystems are of a biochemically totally different nature than vice versa. While biomass rich in proteins and LC-ω3PUFA is transferred to land, e.g., by trophic relationships, the link from terrestrial to aquatic ecosystems provides recalcitrant plant carbon, mainly devoid of essential nutrients, fuelling detrital food chains. Recent global changes influence food webs via altered input and transfer of essential biomolecules, but separating the effects of nutrients, CO2, and warming is not trivial. Current evolutionary concepts (e.g., Black Queen, relaxed selection) considering the costs of metabolic production partly explain food web dynamics, especially for vitamins, whereas adaptations to potential oxidative stress seem to be more important for LC-PUFA. Overall, the provision with essential biomolecules is precious for both heterotrophs and auxotrophs. These nutritional valuable molecules often are kept unaltered in consumer metabolism, including their stable isotope composition, offering a great advantage for their use as trophic markers.
Despite the importance for trophic interactions and consumer fitness, a general comprehension of essential biomolecules structuring food webs and driving consumer adaptations is still lacking to date. For example, little is known about the environmental distribution of essential FA, AA, sterols and vitamins, and how ecosystem functions are constrained by their bioavailability. Essential biochemical resources can directly influence consumers' growth and reproduction, and in turn trophic relationships, including food intake or metabolic requirements. Thus, their availability can act as selection pressure on the evolution of consumer populations.
This paper conceptually summarizes current knowledge and potential implications of essential biomolecules on ecosystem dynamics, i.e., their biochemistry and functionality, their availability and transfer within food webs, and their use as trophic markers. A major focus is set on the forces behind environmental distributions, interlinks between ecosystems and alterations due to anthropogenic impacts. Further, evolutionary aspects in the provision of biomolecules and metabolic adaptations are highlighted.
The Role of Essential Biomolecules in the Food Web
Biochemistry and Functionality
Among FA, ω3- and ω6PUFA are essential for many animals. Unlike plants and higher fungi, whose methyl-end desaturases introduce double bonds in C16- and C18FA at the ω3 and ω6 position, animal desaturases work toward the carboxyl-end beyond the ω6 position (Sprecher et al., 1995; Monroig and Kabeya, 2018). This results in characteristic “ω families,” i.e., ω3, ω6, ω9 (Figure 1). For animals the primary essential dietary derived PUFA of the ω6 family is linoleic acid (LA: 18:2ω6), and of the ω3 family α-linolenic acid (ALA: 18:3ω3). LA and ALA are the precursors for the respective LC-PUFA, also called highly-unsaturated fatty acids (HUFA), obtained by chain elongation and further desaturation (Figure 1). Conversion rates among PUFA, especially from ALA to eicosapentaenoic acid (EPA: 20:5ω3) or docosahexaenoic acid (DHA: 22:6ω3), are low (Stanley-Samuelson et al., 1987; Bell and Tocher, 2009). For instance, only around 5% of ALA are converted to EPA in omnivorous vertebrates, including humans (Davis and Kris-Etherton, 2003). Dietary provision with EPA and DHA can directly enhance consumers' growth, health and fitness (e.g., humans—Hulbert et al., 2014; Nwachukwu et al., 2017; insectivorous birds—Twining et al., 2016; soil microarthropods—Menzel et al., 2018). Therefore, LC-ω3PUFA are classified as semi-essential (Müller-Navarra, 1995a), and LC-ω3PUFA supplementation, e.g., produced via metabolic engineering (Gong et al., 2014), is recommended for humans.
Figure 1. Major pathways in synthesis of long-chain polyunsaturated fatty acids (LC-PUFA) in eukaryotic organisms (modified after Sprecher et al., 1995). LA, linoleic acid; ALA, α-linoleic acid; ARA, arachidonic acid; EPA, eicosapentaenoic acid; DHA, docosahexaenoic acid; dd, direction of the enzymatic desaturation in the fatty acids molecule; methyl-end desaturases introduce double bonds in C16- and C18-FA at ω3 and ω6 position, animal desaturases work toward the carboxyl-end beyond the ω6 position.
LC-PUFA have several key physiological functions in animals. They are an integral part of biological membranes and maintain their adequate viscosity and selective permeability (Vance and Vance, 2002). Further, γ-linolenic acid (GLA: 18:3ω6), arachidonic acid (ARA: 20:4ω6) and EPA serve as precursor for tissues hormones such as eicosanoids, which mediate inflammatory processes, immune response or cell growth (Stanley and Kim, 2019). Moreover, EPA and DHA are concentrated in nervous tissue, being the dominant FA of brain lipids (Wiktorowska-Owczarek et al., 2015). Differences in PUFA requirements exist depending on the consumer taxonomic affiliation, its ontogenetic stage and especially egg production (for zooplankton: Brett et al., 2009), which can affect trophic interactions (Müller-Navarra, 2008). Overall, the dietary LC-PUFA content is critical for growth, reproduction, and neural development for many aquatic and terrestrial invertebrates as well as vertebrates, including humans (e.g., Stanley-Samuelson et al., 1988; Parrish, 2009; Hulbert and Abbott, 2012).
The main ω3- and ω6PUFA producer in aquatic systems are eukaryotic algae (Table 1). In particular, the synthesis of LC-ω3PUFA in algae is tightly connected to photosynthesis, because they are part of the glycolipids in thylakoid membranes of chloroplasts (Guschina and Harwood, 2009). Similar to accessory pigments, LC-PUFA play a role in the light harvesting process. Systematic affiliation seems to be the strongest determinant of PUFA distribution in seston (Müller-Navarra et al., 2004), a finding also reported from cultures (Cobelas and Lechado, 1989; Ahlgren et al., 1992; Galloway and Winder, 2015; Taipale et al., 2016a). However, environmental factors including nutrients, temperature, salinity and light also directly affect the PUFA pattern of algae (Guschina and Harwood, 2009). While LC-ω3PUFA compositions in algae based on relative proportions already assigns group specific pattern (Galloway and Winder, 2015; Peltomaa et al., 2017), differences based on absolute amounts are much more pronounced (data by Cobelas and Lechado, 1989; Ahlgren et al., 1992; Müller-Navarra, 1995b; Jónasdóttir, 2019) and important for the availability to consumers.
Table 1. Essential biomolecules within the groups of fatty acids, sterols, vitamins, and amino acids.
Due to their high absolute EPA content, diatoms are the greatest EPA supplier, both in most marine and freshwater (except dystrophic) systems, followed by chryptophytes, haptophytes, dinophytes and eustigmatophytes (Table 1). From their absolute DHA content, dinophytes are the main supplier, followed by haptophytes. However, certain diatoms as well as most dinophytes are too big to be ingested by most zooplankton. Moreover, heterotrophic stramenopiles (e.g., thraustochytrids) used in pharmaceutical DHA production (Gupta et al., 2012) may be a so far underestimated DHA provider. Heterotrophic eukaryotes can also contribute to sestonic EPA (e.g., ciliates—Bec et al., 2010; Hartwich et al., 2012), converting ALA mainly supplied by chlorophytes and cryptophytes to EPA, i.e., trophically up-grading sestonic food quality for zooplankton. Cyanobacteria generally do not contain LC-PUFA, although some taxa comprise C18-PUFA (e.g., ALA) but at low absolute concentrations (Table 2). Prokaryotes are usually not a source of LC-PUFA, although they occur in bacteria in deep-sea isolates, which is probably an adaptation to low temperature and high pressure in the habitat (DeLong and Yayanos, 1986). Macro-algal chlorophytes display a FA pattern similar to their micro-algal counterpart, while marine rhodophytes have an especially high share of EPA (but none or low DHA) and phaeophytes comprise intermediate levels of LC-PUFA (Fleurence et al., 1994; Pereira et al., 2012).
Table 2. Proportion of polyunsaturated fatty acids (PUFA in % of total fatty acids) in the neutral lipids of photoautrotrophic microbiota dominant in terrestrial soil crusts.
Vascular plants are considered as the major source for PUFA in terrestrial food webs and predominantly contain C18-PUFA, i.e., ALA and LA. Herbivores such as ruminants can acquire LC-ω3PUFA via ciliates as gut symbionts (Veira, 1986; Newbold et al., 2015), which may be able to convert ALA to EPA, like certain ciliates in aquatic systems. Primary producers in biological soil crusts (green algae and cyanobacteria) synthesize ALA, with green algae additionally comprising the PUFA 16:3ω3 as a potential precursor (Buse et al., 2013; Table 2). However, the role of biological soil crusts as ω3PUFA supply for terrestrial food webs has not been explored yet. Among heterotrophs higher fungal taxa commonly synthesize ALA (Ruess and Chamberlain, 2010), moreover lower soil fungi can supply LC-ω3PUFA, predominantly Chytridiomycetes and Oomycetes (Lösel, 1988), and arbuscular mycorrhiza fungi (Gladyshev et al., 2013). Further, there is evidence that many soil invertebrates provide LC-ω3PUFA (see Figure 3, and chapter ω3PUFAs—aquatic vs. terrestrial food webs).
Trophic Transfer and Biomarkers
The importance of EPA and DHA for food quality affects biomass trophic transfer in aquatic ecosystems (Müller-Navarra, 1995a; Brett and Müller-Navarra, 1997; Müller-Navarra et al., 2000). PUFA itself can be as twice as efficiently transferred from the first to the second trophic level compared to bulk carbon (Gladyshev et al., 2011; Mayor et al., 2011). LC-ω3PUFA are particularly retained and accumulated in consumer lipids of aquatic food webs (Strandberg et al., 2015; Guo et al., 2016), which is also a central issue in aquaculture (e.g., Navarro et al., 2014). Generally, fatty acids from the diet can be incorporated into consumer body tissue without major modification, a fact called “dietary routing” (Stott et al., 1997). Based on this, ω3PUFA were used as qualitative markers for trophic interactions in freshwater plankton (Desvilettes et al., 1997), and semi-quantitatively in food webs in marine pelagial (Dalsgaard et al., 2003) and benthos (Kelly and Scheibling, 2012). By applying metabolic conversion factors, dietary routing was traced quantitatively (Iverson et al., 2004) in vertebrates connected to the marine food chain, e.g., for arctic mammals (polar bears—Thiemann et al., 2008) or sea birds (Williams and Buck, 2010). Further, Galloway et al. (2015) employed a Bayesian approach (FA source-tracking algorithm) comparable to the use of stable isotopes in food web ecology. This wide application of lipids as trophic markers in aquatic habitats has benefitted from the frequent occurrence of ω3PUFA in primary producers at the food web base.
In contrast, the use of FA biomarker in terrestrial food webs has lagged behind. First trophic transfer of fatty acids was assigned in detrital food chains in soils from bacteria and fungi to microbial grazers (nematodes—Ruess et al., 2002; Collembola—Haubert et al., 2006) and further up to omnivores and predators (Collembola—Ruess et al., 2004; spiders—Pollierer et al., 2010). Opposite to aquatic ecosystems, this was based on the dietary routing of non-essential FAs, e.g., methly-branched and cyclic forms derived from bacteria (Ruess and Chamberlain, 2010). The achievement of comparable results in the herbivore food chain was hindered by the lack of LC-ω3PUFA in terrestrial primary producers, resulting in ALA as major biomarker for plant feeding (Ruess and Chamberlain, 2010) and C16-ω3PUFA for algal feeding (Buse et al., 2013). However, this drawback of lower diversity in FA markers can be overcome by applying stable isotope fingerprints, tracing FA dietary routing via their δ13C signal. Here, main approaches are 13CO2 pulse-labeling of plants (Pausch et al., 2016) or using natural differences in 13/12C ratios of C3 and C4 plants (Haubert et al., 2009; Ngosong et al., 2011) (Figure 2). However, a broader application of FA in food web ecology of vertebrates, as common in marine systems, is still lacking, except of the usage of FA markers in food chemistry (Molketin and Giesemann, 2007). For an overview on trophic transfer and biomarkers in terrestrial systems see reviews of Ruess and Chamberlain (2010) and Traugott et al. (2013).
Figure 2. Carbon stable isotope fingerprinting in aquatic and terrestrial food webs based on differences in δ13C of primary producers. Left—δ13C content in bulk tissue of major resources and in non-essential and essential amino acids of Atlantic blue crabs (Callinectes sapdius) in bay and marsh habitats (data from Fantle et al., 1999). The difference in δ13C between primary producers or amino acid fractions is expressed as Δ13C. Right—fractionation (Δ13C) in linoleic acid (18:2ω6,9) between Collembola (Orchesella villosa, Protaphorura fimata) and soil fungi in a C3 (soya) and C4 (maize) arable system with different farming practice (data from Haubert et al., 2009). No fractionation indicates dietary routing of linoleic acid and hence fungal-feeding. Values with the same letters are not significantly different according to Tukey HSD (P < 0.05).
Biochemistry and Functionality
Sterols are an important lipophilic part of cell membranes in eukaryotic organisms, embedded within the membrane phospholipids. Moreover, they are frequently esterified to membrane LC-PUFA. The central sterol synthesized in animals is cholesterol, a C27 sterol. However, not all animals are capable of de novo sterol synthesis. For example, arthropods lack this ability (Goad, 1981; Martin-Creuzburg and von Elert, 2009), and many insects and crustaceans prefer Δ5 and Δ5, 7 over Δ7 and Δ22 sterols (e.g., Teshima, 1971; Behmer and Nes, 2003). Known from herbivorous insects and crustaceans, dietary phytosterols are typically altered by de-alkylation and saturation, e.g., of C24 methyl and ethyl sterols, to form cholesterol (Svoboda and Thompson, 1985). Despite this, sterol limitation was shown for crustaceans feeding on laboratory cultures of heterotrophic and autotrophic bacteria (e.g. Martin-Creuzburg et al., 2011 for Daphnia) or diatoms (Hassett, 2004 for Acartia, Calanus). However, interacting effects of sterols with the provision of EPA (Martin-Creuzburg et al., 2009 for Daphnia) or AA (Wacker and Martin-Creuzburg, 2012 for a rotifer) were also demonstrated. Nevertheless, a minor part of sterols (less than 1%) is required as precursor for molting hormones in arthropods (e.g., ecdysteroids; Svoboda and Thompson, 1985).
In vertebrates, 7-dehydrocholesterol is converted to cholecalciferol (vitamin D3) under UV irradiation and functions as steroid hormone in the Ca-metabolism, with special importance for skeleton structures, e.g., in humans (DeLuca, 1998). Except for hormone production, sterol requirements of many organisms seem not to be specific. Additionally, the metabolic modification of dietary sterols widens sources for organisms with a low or lost ability of de novo synthesis.
In planktonic food webs, eukaryotic macro- and micro-algae are very variable sources of over 250 different sterols (mainly C28 phytosterols) (Santos et al., 2015) (Table 1). However, their distribution within an algal class is not as uniform as for PUFA (e.g., Volkman, 1986, Martin-Creuzburg and Merkel, 2016; Taipale et al., 2016a). Prokaryotic planctomycetes and poribacteria have the genetic infrastructure for sterol synthesis (Pearson et al., 2003) but their role in dietary sterol supply is unknown. Eukaryotic fungi are potentially an important resource in aquatic ecosystems, especially in streams (Krauss et al., 2011). The same applies to chytrids, ubiquitous fungal parasites in aquatic ecosystems, providing a sterol source to their grazers even in absence of their phytoplankton hosts (Gerphagnon et al., 2019). Cyanobacteria as prokaryotes do not produce sterols at all (Volkman, 2003).
In terrestrial ecosystems, higher plants deliver mainly C28 and C29 sterols (Moreau et al., 2018) e.g., by leaves, fruits, roots and bulbs to herbivores, both in above- and belowground food webs (Table 1). Fungi are also frequent sterol producers in soil systems (Burden et al., 1989), contributing ergosterol as a major component of their cell membranes (Joergensen and Wichern, 2008). If and how these fungal sterols can act as a nutrition source for soil animals has yet to be explored. Finally, symbiotic fungi in the gut may provide a substantial part of sterols to their insect host (reviewed by Douglas, 2009).
Trophic Transfer and Biomarkers
Phytosterols are metabolic converted by several herbivorous consumers to suit specific physiological requirements, hampering their trophic biomarker usage. Above, many animals—especially vertebrates—are capable of de novo sterol synthesis, which makes sterol limitation further up the food chain unlikely, especially in the 3RD and 4TH trophic level of both, aquatic and terrestrial food webs. However, a comprehensive understanding is still lacking.
Metabolic sterol processing was reported, e.g., for heterotrophic protists feeding on macro-algae (Chu et al., 2009), soil nematodes feeding on plant roots (Chitwood and Lusby, 1991; Chitwood, 1999), millipedes feeding on terrestrial plant litter (Rawlins et al., 2006), and crustaceans feeding on phytoplankton (Martin-Creuzburg and Merkel, 2016 for Daphnia). Additionally, biochemical sterol modulation generally occurs is herbivore insects (Svoboda and Thompson, 1985). However, the suitability of phytosterols may differ (Martin-Creuzburg et al., 2014 for Daphnia; Gergs et al., 2015 for gammarids), and not all zooplankton consumers do convert those (Wacker and Martin-Creuzburg, 2012 for rotifers). Although the less group-specific occurrence of phytosterols in algae and their conversion in many herbivores are hampering their sole application as trophic markers in pelagic food webs, sterols together with FA as markers seem promising to track food intake, as shown for dwelling ophiurids and holothurians in a deep-sea environment (Drazen et al., 2008). In general, sterols are widely used as biomarkers in sediments due to their chemical persistence, e.g., separating allochtonous and autochtonous produced biomass (Bianchi and Canuel, 2011).
Biochemistry and Functionality
Vitamins are a diverse class of rather complex compounds, and from the two major groups only the most important in food web ecology are considered here:
Lipid soluble vitamins (A, D, E)
Vitamin A is essential for animals and primarily needed for vision. Carotenoides (provitamin A) are synthesised in chloro- and chromoplasts of photoautotrophic organisms as photoprotecting agent (Saini et al., 2015; Huang et al., 2017). Vitamin E is an anti-oxidant protecting susceptible LC-PUFA, and requirements in animals are connected to PUFA provision (Zhang et al., 2017). This protective function may also be related to the transition from parthenogenetic to sexual reproduction, male fertility (spermatogenesis) and enhanced growth of the mictic offspring as shown for the rotifer Asplanchna by Gilbert (1980). Vitamin D is a derivate from cholesterol and considered in the chapter on sterols above.
Water soluble vitamins (B-group)
B1 (thiamin) is a cofactor of several core enzymes, e.g., in the transfer of C2-groups (dehydrogenases, decarboxylases) in the carbohydrate metabolism. Requirements of external B1 are mostly due to the lack of either synthesis of the pyrimidine or the thiazole moiety in algae (Lewin, 1961). If capable of biosynthesis, thiamin is only produced on demand via riboswitches, both in prokaryotes and eukaryotes (McRose et al., 2014), making the process very efficient. Physiological interconnections exist with other vitamins, e.g., folic acid (B9) deficiency influences B1 adsorption and metabolism (Wolak et al., 2017). Further, supply in B1 can alter the FA pattern towards EPA and DHA, e.g., in the alga Rhodomonas baltica (Chi et al., 2018).
B7 (biotin) requirements are known for some crysophytes, dinophytes, and euglenoid algae (Provasoli and Carlucci, 1974). Folic acid (B9) is synthesized by plants, including algae (Baker et al., 1981), but is essential to animals as a cofactor of thymidyl-synthase, catalyzing nucleotide syntheses, which governs DNA repair and replication.
B12 (cobalamin) is a cofactor in enzymes carrying activated methyl groups or providing carbon-based free radicals for reactions removing non-acid hydrogen atoms (Marsh, 1999). It is involved in the synthesis of AA and DNA, and in shuffling C1-groups into the citrate circle. Two synthesis pathways exist, i.e., the more ancient anaerobic pathway of bacteria and Archaea leading to cobalamin, and the aerobic pathway of cyanobacteria resulting in pseudo-cobalamin (Raux et al., 1999). Cobalamin cannot be synthesized by most eukaryotes, including animals (Gräsbeck and Salonen, 1976). Overcoming potential limitations due to B12 auxotrophy seems to be governed by a non-cobalamin methionine synthase in higher plants and certain algal taxa (Croft et al., 2006). Moreover, B1 deficiency syndromes in fish (Marcquenski and Brown, 1997) and sea birds (Balk et al., 2009) may be coupled to B12 shortage in resources. Overall, the metabolic pathways of B1, B9, B12 and the AA methionine are interwoven, and also relevant on the ecological level by impacting nitrogen (N) and sulfur metabolism of eukaryotic phytoplankton (Bertrand and Allen, 2012). This makes it difficult to determine the vitamin that is the most limiting (Table 1).
Lipid soluble vitamins
The syntheses of the lipophilic vitamins A and E are tightly connected to the metabolic capacity of algae in aquatic (Huang et al., 2017) and of plants in terrestrial (Saini et al., 2015) ecosystems. In marine and freshwater, microalgae as well as makrophytes represent the dominant source (Cuvelier et al., 2003; Huang et al., 2017) (Table 1). Pro-vitamin A dominates in leaves and fruits, whereas seeds comprise the highest amounts of vitamin E, and leaves of vitamin K (Aseni-Fabado and Munné-Bosch, 2010). Fungi and yeast are major producer of ergosterol, the precursor of ergocalciferol (i.e., pro-vitamin D2), but UVB exposure is necessary for conversion, restricting the supply to aboveground habitats. Traditionally higher plants were thought to contain only negligible amounts of D3 but recent work raises evidence for a broader distribution (Jäpelt and Jakobsen, 2013). Whether these contents are sufficient to subsidize decomposer food webs in lightless soil habitats remains to be explored.
Water soluble vitamins
In aquatic systems, red and green algae are a good source of B vitamins, especially B1, and B9 (Croft et al., 2006) (Table 1). In contrast, main B12 producer seem to be ammonium oxidizing thaumarchaeota, primarily under cold conditions, i.e., at greater depth, during winter and in polar-regions (Doxey et al., 2015). Interestingly, most algae—especially those groups known to provide LC-ω3PUFA to food webs—are only minor vitamin B suppliers, as many of them are auxotroph in respect to B1 (20%), B7 (5%) and especially B12 (50%) (Provasoli and Carlucci, 1974; Croft et al., 2006). Although cyanobacteria are rich in B1, they are an inefficient source of B12 as they only contain the nutritionally inferior pseudo-cobalamin (Helliwell et al., 2016).
In terrestrial systems, higher plants are the major producers of B-vitamins (Roje, 2007), delivering these water-soluble vitamins via root exudation into the rhizosphere and additionally supporting their mycorrhiza symbionts (Grayston et al., 1996) (Table 1). The second important vitamin B sources are soil bacteria, with phosphate-solubilising taxa azotobacters and rhizobia as significant producers (Vranova et al., 2013). The cumulative vitamin production by bacteria in the rhizosphere enhances general bioavailability and complements root exudates (Baya et al., 1981), likely important for the associated fungi and fauna.
Trophic Transfer and Biomarkers
Lipophilic vitamins synthesized by algae or vascular plants are generally transferred to heterotrophic consumers via predator-prey interactions. In contrast, syntrophic relationships with microbes seem to be important to overcome certain vitamin B limitations, as shown for marine algae co-cultured with bacteria (Paerl et al., 2015). Beneficial microbe-algae (Croft et al., 2005) and algae-algae interactions (Carlucci and Bowes, 1970; Baker et al., 1981) seem rather to be the rule than the exception. However, their role in overcoming B12 limitation sustaining global primary production is debated (e.g., Droop, 2007). In nature, B12 is acquired from soluble surroundings with specific transporters by B12 auxotrophic algal cells (Bertrand and Allen, 2012), ensuring rapid uptake. For food webs of marine pelagic systems there is evidence that B1 is not accumulated but rather diluted from phytoplankton to zooplankton to fish (Sylvander et al., 2013).
In aquatic ecosystems, B12 provision by endosymbionts is known for certain ciliates (Baker et al., 1981). More recently, Fiore et al. (2015) showed symbiotic interactions with Archaea and bacteria to be crucial for the Caribbean giant barrel sponge (Xestospongia muta) in obtaining B-vitamins and essential AA. So far, mutualistic relationships of sponges or corals are rather viewed in the light of carbon acquisition but should also be connected to the acquisition of essential biomolecules. In contrast to aquatic ecosystems, the importance of gut symbionts as suppliers of vitamins to their terrestrial vertebrate and invertebrate hosts has been recognized for a long time, especially for bacteria or ciliates as endosymbionts in social insects such as wood feeding termites or insects that suck on plant sap, which is poor in vitamins (Moran et al., 2003; McCutcheon et al., 2009). B2 is provided by gut bacteria to earthworms (Sulik et al., 2012) or by the mutualistic Wolbachia bacteria to nematodes (Taylor et al., 2012). Moreover, the intestinal flora plays a major role in the provision with B7, as shown for humans (Magnúsdóttir et al., 2015). Overall, the provision with B vitamins by mutualistic prokaryotes in invertebrates and vertebrates as “hidden” trophic interactions complicates determination of their trophic transfer in food web studies.
Biochemistry and Functionality
AA are the structural elements of enzymes, regulating key metabolic pathways important for health, survival and growth, e.g., neurological and immunological functions (Wu, 2010). Traditionally, AA are classified as none-essential (dispensible) and essential (indispensible). The former can be de novo synthesized by the consumer, whereas the later must be provided with the diet. Nine AA have been assigned as essential in humans and other vertebrates, i.e., isoleucine, histidine, leucine, lysine, methionine, phenylalanine, threonine, tryptophan, and valine (Young, 1994), yet requirements vary between taxonomic entities. In addition, arginine is essential for terrestrial carnivores (Morris, 1985). A third category is named conditionally indispensable or “functional” AA, which are semi-essential as synthesis rates in certain taxa are limiting (Wu, 2010). A relevant example is arginine in many mammals (Wu et al., 2013). The metabolic flexibility in consumers, such as compensatory mechanisms can affect AA limitation. Only recently, the upregulation of AA retention efficiency as a response to nitrogen deficiency was shown in copepods (Burian et al., 2018). In conclusion, we are still at the start of understanding which AA are essential in different animal groups, and what implication this dependency has for food web ecology.
In aquatic food webs, phytoplankton, particularly protein-rich algae (above 50% dry weight - Bleakley and Hayes, 2017) are a main source for AA (Table 1). Aquatic macrophytes, in contrast, display a much lower protein (Rather and Nazir, 2015) and consequently AA content, due to more structural components (cellulose, hemicellulose, lignin). Terrestrial plants, their leaves, flowers and fruits provide AA to herbivores in terrestrial food webs (Takizawa et al., 2017). However, AA levels are typically low and supply often needs to be enriched via mutualistic interactions with gut microbiota in herbivores (Cantalapiedra-Hijar et al., 2016 for lambs). Microbial derived proteins further represent an important resource for essential AA in detritivore food webs as shown by Steffan et al. (2017) analyzing invertebrates (moths, beetles) and vertebrates (fish). Degradation of plant litter by bacteria and fungi provide AA for detrivores (Larsen et al., 2009). Protein is hydrolysed via extracellular enzymes, followed by adsorption of free AA from the soil solution (Czimcik et al., 2005). Particularly bacteria, which can acquire AA by both, de novo synthesis using inorganic nitrogen, and by direct incorporation of organic substrates, comprise diverse AA (McMahon and McCarthy, 2016). Moreover, AA can be derived from endo-symbiotic gut bacteria, e.g., in earthworms and enchytraeids (Larsen et al., 2016) or intracellular co-symbionts like Buchnera in nematodes and insects (Moran et al., 2003; McCutcheon et al., 2009).
Trophic Transfer and Biomarkers
In contrast to terrestrial systems, protein limitation per se is rather unlikely in pelagic aquatic systems, but certain essential AA may become in short supply (review by Müller-Navarra, 2008). Moreover, trophic transfer of AA can be impaired by co-limiting resources such as sterols (Wacker and Martin-Creuzburg, 2012 for a rotifer). In addition, a meta-analysis of zooplankton across 29 oligotrophic lakes by Guisande et al. (2003) revealed taxa specific AA composition, likely indicating distinct food sources.
The AA composition of primary producers can be markedly different to their animal consumers or microbial degraders (Steffan et al., 2015; Takizawa et al., 2017), offering great potential to follow the transfer of specific AA along the trophic cascade. Two AA categories are distinguished as biomarker in food web ecology: The so called “source” AA exhibiting small 15N-discrimination but preserve the 15N/14N ratio (δ15N) of the food (McMahon and McCarthy, 2016), while the amino-N of “trophic” AA is routinely exchanged in the metabolic pool (O'Conell, 2017). Thus, 15N of “trophic” AA is enriched along the trophic cascade (McMahon et al., 2016) (see Table 3). However, it is important to note that the categorization in “source” and “trophic” AA is based on differences in cycling of the N moiety and not on changes within the carbon skeleton. The latter is distinguishing essential and non-essential AA, respectively. The respective parameters and calculations to assign trophic positions by the stable isotope signal of AA are summarized in Table 3.
Table 3. “Trophic” and “source” amino acids, fractionation factors, and formula used in in food web studies (Modified after McMahon and McCarthy, 2016).
The broadest biomarker application received the AA couple glutamic acid (Glu; trophic) and phenylalanine (Phe; source). The underlying assumption is that the isotopic fractionation is constant across binary links with the trophic discrimination factor (TDFGlu−Phe) being 7.6‰ (Chikaraishi et al., 2007) (Table 3). TDFGlu−Phe was successfully applied to assign trophic positions of consumers in very different trophic relationships. These comprised arthropod functional groups in orchard food webs, ranging from sap-feeding herbivores over parasitoids and hyperparasitoids to predators (Steffan et al., 2013) as well as food chains with a broad phylogenetic spectrum, ranging from bacteria and fungi over insects to mammals (Steffan et al., 2015). However, recent work questions a single fixed value for TDFGlu−Phe and reports variability from 0 to 10‰ depending on diet quality, consumer nitrogen excretion, and trophic level (Nielsen et al., 2015; McMahon and McCarthy, 2016; O'Conell, 2017; Pollierer et al., 2019).
Another premise in applying δ15N of AA in food web ecology is the absolute term “β”, the difference in δ15N of AA in primary producers at the base of food webs (Table 3). For example, in primary producers, δ15N of AA in floral biomass seem to depend on the absence or presence of active photosynthesis (Takizawa et al., 2017). At the consumer level interspecific differences in prey organisms may also lead to AA imbalance and subsequently variation in AA δ15N (Ventura and Catalan, 2010 for different crustaceous zooplankton) or increased AA losses by N excretion (Saavedra et al., 2015). The βGlu/Phe (Table 3) was initially proposed to be −3.4‰ for coastal marine and +8.4‰ for terrestrial primary producers (Chikaraishi et al., 2010) but variation in “β” occurs, and its combination with δ13C in bulk tissue is recommended to enhance resolution (Choi et al., 2017).
Generally, inter-trophic AA 15N discrimination seem to be similar among bacteria, fungi and animals (Steffan et al., 2015), whereas the δ15C of essential AA exhibited very different pattern between plants and bacteria or fungi (Larsen et al., 2009). This allows enhancing the resolution in the application of AA as trophic markers by using their isotopic C signal. Stable isotope fingerprinting of 13C/12C in AA is particularly successful in habitats where primary producers display distinctly different 13C signals (Figure 2). This approach was used to identify plant, fungal or bacterial origin of AA (Larsen et al., 2009), feeding habits of the Atlantic blue crab (Fantle et al., 1999) as well as movement and foraging ecology of birds (McMahon et al., 2015b). Only recently, this approach was employed to quantify the trophic levels and the basal resources in soil detritivores (earthworms, Potapov et al., 2019) as well as predators (gamasid mites, spiders; Pollierer et al., 2019). Overall, there is sufficient evidence that the “trophic” and “source” concept is pertinent for many organisms, yet a quest for a single TDF or “β” value may not hold across food webs and ecosystems. Factors such as AA limitation or excretion can lead to mismatches in biochemical stoichiometry, which calls for more physiological and environmental studies to improve the application of AA in trophic ecology.
Forces Behind Environmental Distribution
Natural Environmental Conditions
There are vast differences in the comprehension of what drives the distribution of essential biochemicals in ecosystems with the least known about AA and for terrestrial systems. In aquatic habitats, strong negative correlations between total phosphorus and the lakes' summer seston content of EPA and DHA—but not ALA—were reported (Müller-Navarra et al., 2004; Table 1). Those were connected to the relative abundances of algal groups (Müller-Navarra et al., 2004; Sushchik et al., 2014) and—via trophic transfer—could even be detected in top predators, such as perch (Taipale et al., 2016b, 2018). The whole years' distribution of PUFA is, however, more complex (Gladyshev et al., 2007). In addition, temperature and light can alter seston PUFA directly as shown for EPA in a clear water lake by Hartwich et al. (2012). Humic substances in dystrophic lakes may shield susceptible LC-PUFA from UV, but also exert direct toxic effects to consumers, such as daphnids (CasaNova et al., 2018 and references therein). Salinity gradients structuring estuaries can affect trophic dynamics of LC-ω3PUFA, especially in larval fish (Litchi et al., 2017).
Vertical distributions of PUFA and sterols differ in particulate organic matter of aquatic ecosystems. Generally, LC-PUFA are depleted and sterols enriched during sinking, mainly because of the high susceptibility of LC-PUFA but high persistency of sterols against degradation (Wakeham and Canuel, 1986). Many profundal habitats depend on pelagic provision with PUFA, e.g., when algae blooms perish (Ahlgren et al., 1997), and consumers have adapted to this low availability. For example, benthic harpactoid copepods have a more efficient conversion of C18-PUFA to the respective LC-PUFA than pelagic calanoid copepods (Nanton and Castell, 1998). Aquatic phanerogams contain only ALA and allochtonous carbon is devoid of nutritional LC-PUFA alongside protein (Brett et al., 2017).
Pronounced differences also exist in the distribution of B12 in aquatic ecosystems with Archaea preferentially producing B12 in cold areas and times of the year (Doxey et al., 2015). Primary production can be B12 limited in high-nutrient low-chlorophyll areas (Koch et al., 2011 for Gulf of Alaska), and the competition for B12 between eukaryotic algae and heterotrophic bacteria impact total phytoplankton quantity, species composition and succession (Koch et al., 2012). The vitamins B1, B7, and B12 seem to co-act in controlling algal succession and blooms in the ocean (Sañudo-Wilhelmy et al., 2006, Gobler et al., 2007). Occurrence of harmful algae blooms in marine systems may be favored by high vitamin B presence, as especially toxin-producing chryso- and dinophytes are vitamin B auxotrophs (75% B1, 37% B7, and 100% B12; Tang et al., 2010). In freshwater systems, algal blooms dominated by cyanobacteria reduce resource quality at the food web base. Cyanobacteria lack LC-ω3PUFA and sterols, their pseudo-cobalamin is no source of B12 for most herbivores, and, moreover, they potentially contain toxins.
ω3PUFA—Aquatic vs. Terrestrial Food Webs and Interlinks
In contrast to aquatic systems with a predominant supply of LC-ω3PUFA (EPA, DHA) by micro-algae, higher plants as major primary producers in terrestrial ecosystems provide only C18-ω3PUFA (ALA; Figure 3). This questions the main origin of LC-ω3PUFAs in terrestrial food webs. The potential of aquatic derived LC-ω3PUFA to subsidize terrestrial ecosystems was first estimated by Gladyshev et al. (2009). Trophic transfer to land can occur when terrestrial predators (bears, herons, eagles; Figure 3) directly feed on aquatic animals (molluscs, crustaceans, fish). The same applies when terrestrial predators (swallows; Twining et al., 2016) feed on terrestrial stages of prey with both, aquatic and terrestrial life stages (e.g., after insects' emergence; Borisova et al., 2016). In addition, the wax and wane of flooding events (Junk et al., 1989), with algal production in temporary shallow water habitats of riparian areas, is a crucial source of LC-ω3PUFA. In sum, aquatic systems are currently considered a major origin of LC-ω3PUFA for residential terrestrial animals, including humans (Gladyshev et al., 2013; Hixson et al., 2015; Colombo et al., 2017) (Figure 3).
Figure 3. Proposed origin of long-chain polyunsaturated fatty acids (LC-PUFA) in terrestrial ecosystems. Left—transfer to land via different trophic levels of the aquatic food chain is commonly regarded as major input; right—soil decomposers are a neglected source. Please note that “hidden” channels such as mutualistic gut microbiota in e.g., earthworms or ruminants, are not specifically emphasized. ALA, α-linolenic acid; EPA, eicosapentaenoic acid; DHA, docosahexaenoic acid. Illustration credit: https://vecteezy.com.
However, this hypothesis is controversial. For example, the highest DHA contents were not found in water birds, such as waterfowls feeding in aquatic habitats, but instead, in terrestrial feeders such as Passeriformes species (Gladyshev et al., 2016). Correspondingly, Fontaneto et al. (2011) suggested terrestrial insects, which besides ARA and ALA also comprise EPA, as a better source for LC-PUFA than aquatic insects due to their higher abundance and accessibility to terrestrial consumers. Moreover, the contribution of ω3PUFA derived from photosynthetic microalgae in biological soil crusts (Table 2) to food webs in nutrient poor and dry desert, dune and tundra habitats remains to be explored.
A so far neglected source of LC-ω3PUFA in terrestrial ecosystems is the soil fauna (Figure 3). Across a wide taxonomic range of soil invertebrates the capability to synthesize LC-ω3PUFA de novo was shown. The entire set of desaturases and elongases to produce LC-ω3PUFA occurs in the nematode Caenorhabditis elegans (Watts and Browse, 2002). Recent molecular studies proved the presence of ω3FA desaturase enzymes in several other free-living soil nematode taxa (Menzel et al., 2019) as well as in terrestrial oligochaetes and insects (Kabeya et al., 2018). EPA synthesis was further indicated for soil Collembola (Menzel et al., 2018) and earthworms (Petersen and Holmstrup, 2000).
Proportions of EPA in total fatty acids reported are 3.5% for free-living soil nematodes (Kühn et al., 2018) and up to 17.4% for yeast feed Collembola (Chamberlain and Black, 2005). In particular, earthworms (their body, gut and burrow lining) are a rich source for LC-ω3PUFA, with EPA being 7.5 times higher than in bulk soil (Sampredo et al., 2006). This represents a considerable source irrespective of whether LC-ω3PUFA are acquired by the animal itself or from gut microbiota. Comparable to aquatic food webs, EPA seems to be selectively retained in soil decomposer food chains as suggested by the occurrence in top predator such as centipedes and spiders (Pollierer et al., 2010; Ferlian et al., 2012). In sum, there is sufficient evidence that belowground biota build central deposits for essential LC-ω3PUFA, which can fuel higher trophic levels above ground (Figure 3).
Since humans have settled, they preferentially modulated riparian areas, which have a central role in LC-ω3PUFA production and export to land, thereby altering the ecological availability of these nutritional valuable biomolecules. A more recent anthropogenic impact is global climate change, i.e., elevated atmospheric CO2 and temperature. Temperature changes act predominantly on PUFA, due to their central role in maintaining membrane fluidity in poikilothermic species (Hazel, 1995). The proposed food web impacts of increased temperature focus on a general decline of LC-ω3PUFA in aquatic primary producers (e.g., Hixson and Arts, 2016). However, extrapolating temperature effects observed for algal cultures to a potential worldwide reduction in sestonic LC-ω3PUFA may be misleading. As algal group composition mainly drives ω3PUFA content, all factors altering community structure, including nutrient regimes and their interactions (Suikkanen et al., 2013) need to be considered, not solely temperature. A recent statistical model predicts a 12% decline of EPA in top predator fish at increasing ocean surface temperatures off Australia, in an area also prone to alterations in nutrient regime (Pethybridge et al., 2015). Moreover, trophic transfer can be impacted by the mismatch in timing rather than by the biochemical composition of the prey (e.g., Seldon et al., 2018). In any case, melting of polar ice with increasing temperatures will affect the occurrence of ice-algae as reliable source of EPA for zooplankton productivity in the Arctic (Leu et al., 2011) and Antarctic (Kohlbach et al., 2017).
In terrestrial plants, the decline of the LC-ω3PUFA precursor ALA with increasing temperature can reach 50% in soybeans (Byfield and Upchurch, 2007) and 77% in rapeseed (Namazkar et al., 2016). On one hand, this is due to low expression of ω3-FA desaturase genes, on the other hand it is induced by general temperature stress that reduces the overall fat and seed biomass. Higher growing temperatures also lower vitamin contents in fruits and vegetables, as shown for vitamin C in kiwi (Richardson et al., 2004) or broccoli (Kumar et al., 2016). With elevated temperature, alterations in PUFA pattern and vitamin contents are expected in herbivores (Adler et al., 2013 for cow milk) accompanied by changes of plant community structure from C3 to less nutritious C4 (Warne et al., 2010). Finally, temperature increase can provoke proteomic responses of microorganisms affecting biosynthesis of essential nutrients in decomposer food chains (Mosier et al., 2015).
The ecological influences of elevated atmospheric CO2 on essential biomolecules in aquatic ecosystems are not uniform, as CO2 can be a potential limiting resource for primary producer but also a stressor by lowering the pH. Ocean acidification can induce phytoplankton community shifts, which negatively influences trophic transfer of essential compounds (e.g., Rosoll et al., 2012). However, larval fish exhibited more whole-body fat at higher CO2, including essential FAs (Díaz-Gill et al., 2015). Studies combining effects of warming and acidification found minor or no changes in the essential AA content in marine diatoms (Bermúdez et al., 2015) but an increase in EPA in primary producer and mesozooplankton consumer (Wang et al., 2017). By using AA-specific δ13C measured in long living deep-sea corals, McMahon et al. (2015a) could detect a shift toward non N2-fixing cyanobacteria during warmer times, i.e., in the Medieval Climate Anomaly and the Industrial Era.
In terrestrial ecosystems, elevated CO2 per se and in combination with temperature increase, reduced ALA and vitamin C contents in fruits, oils and seeds of plants (Kahn et al., 2013; Namazkar et al., 2016). Increased droughts can up-regulate the metabolic pathways for thiamin (B1) reported for Zea mays (Rapala-Kozik et al., 2008), a response to enhance stress tolerance of the plant. Moreover, changes in land use affect the interactions between plants and the soil microbiome, altering vitamin exudation by roots as well as the production by rhizosphere bacteria. For example, herbicides reduced the production of B vitamins in the soil bacterium Azotobacter (Murcia et al., 1997). Overall, such changes in the rhizosphere as a hot spot for diverse microbial communities and, thus, metabolic pathways and substrates, have considerable impact on the occurrence and availability of essential biomolecules for higher trophic levels.
Essential biomolecule physiology recently achieved attention as a trait within evolutionary concepts (reviewed by Ellers et al., 2012). For example, the loss of de novo synthesis of vitamin C in many mammals is connected to ample access by frugivory, leading to “relaxed selection” sensu Lahti et al. (2009). Under “environmental compensation” lost traits can be functionally compensated by others, e.g., in the case of vitamin D dietary provision is substituted by light. According to the “Black Queen Hypothesis,” genes and related traits can be lost as the metabolites are provided as common goods by other members of a consortium (Morris et al., 2012).
Whether these evolutionary concepts will explain the environmental distribution in nutritional valuable molecules on a food web level warrants further investigation. With comparative genomics, Mee and Wang (2012) showed that AA de novo synthesis of Eukarya is restricted to 4.1 AA (humans 11 AA), whereas Archaean on average de novo synthesize 8.3 and bacteria 7.9 out of 20 AA, respectively. Corresponding to the constitutive costs proposed by Lahti et al. (2009), most organisms do not synthesize those AA, which require many biochemical steps, thus are metabolically more costly to produce. Moreover, intra- and extracellular production of AA and vitamins differ between free-living bacteria and biofilms in marine benthos (Johnson et al., 2016), suggesting provision of essential biomolecules by the consortium in line with the “Black Queen Hypothesis.” Essential extracellular metabolites such as AA and vitamins may even be a valuable “currency” in microbial cross-feeding (Seth and Taga, 2014) and for microbial grazers at the base of aquatic and terrestrial decomposer food webs.
The dynamics of ω3- and ω6PUFA in food webs, however, do not fit those evolutionary trait considerations of dependencies through adaptive gene loss. In a phylogenetic study across 54 invertebrate taxa, including Acari, Crustacea, Insecta, and Nematoda, no indication of a link between the dietary availability of LA and its de novo synthesis was detected, rather LA synthesis was facilitated by the bi-functionality of desaturase enzymes (Malcicka et al., 2018). Generally, fewer steps are involved in the synthesis of LC-PUFA than for many other essential biomolecules. LC-PUFA are prone to peroxidation if not protected by antioxidants like vitamin E, with peroxidation products being harmful (Finkel and Holbrook, 2000). This suggests that, in contrast to other nutritional biomolecules, the response to oxidative stress may be the trait here, and the costs are related to features mitigating the damaging effects of LC-PUFA peroxidation (Monaghan et al., 2009). Nevertheless, holding genes such as the Fads2 desaturase to de novo synthesize DHA, is considered important for recurrent freshwater colonization and radiation in fishes (Ishikawa et al., 2019).
Overall, synthesis of specific nutritional biomolecules can be lost by species or whole systematic groups if it is more efficient to obtain those from the environment. This converts them into essential dietary compounds, yet constraints appear to differ according to biochemical susceptibility and synthesis pathways.
Essential biomolecules play an important role in trophic interactions across taxa in aquatic and terrestrial ecosystems. Their availability at the base of the food web matters for the mode of trophic transfer, affecting food web structure as well as response to environmental changes. For example, algae and higher plants as primary carbon fixers do not provide all essential biomolecules, and e.g., Archaea are the main producer of B12. As its' biochemical functioning is tightly connected to other essential biomolecules (B vitamins and methionine), mutual to symbiotic trophic interactions are characteristic for provision. In contrast, LC-ω3PUFA and AA are mainly transferred via predator-prey interactions and their minor metabolic alterations predetermine them for dietary tracing. Particularly in combination with compound-specific stable isotope analyses they provide quantitative estimates of resource flows. Terrestrial and aquatic food webs differ considerably in the amount and distribution of essential biomolecules, e.g., in FAs, and interlinks are important, especially from water to land.
However, our knowledge on the function of essential biomolecules in food webs is far from complete. Future food web research questions to be addressed are: (1) How are food web assemblages in different biomes adapted to the local sources of essential nutritional compounds? (2) Are there considerable exchanges/fluxes in essential compounds between terrestrial herbivore and detritivore food chains? (3) How do food chain loops, such as the microbial loop, contribute to the dynamics of essential biomolecules, besides known trophic-upgrading within PUFA? (4) How does the availability of essential biomolecules affect the organization of biotic consortia, e.g., aquatic biofilms or rhizosphere microbiomes? (5) What is the impact of hidden sources, e.g., gut microbiota, on the reconstruction of food webs using essential biomolecules as trophic markers? (6) What is the general role of essential biomolecules in food web dynamics at higher trophic levels compared to the frequently investigated plant-herbivore interface? Finally, as the capability for de novo synthesis can act as trait in evolution, a new research field opens up, connected to questions on how essential biomolecules can impact adaptations and radiation of species, including the divers trophic interactions—from mutualism to parasitism.
LR and DM-N contributed equally to the conception and writing of the work as well as to its content and interpretation.
We acknowledge support by the German Research Foundation (DFG) and the Open Access Publication Fund of Humboldt-Universität zu Berlin.
Conflict of Interest Statement
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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Keywords: food web, essential biomolecules, fatty acids, amino acids, sterols, vitamins, trophic transfer, environmental distribution
Citation: Ruess L and Müller-Navarra DC (2019) Essential Biomolecules in Food Webs. Front. Ecol. Evol. 7:269. doi: 10.3389/fevo.2019.00269
Received: 02 November 2018; Accepted: 26 June 2019;
Published: 16 July 2019.
Edited by:Monika Winder, Stockholm University, Sweden
Reviewed by:Sami Johan Taipale, University of Eastern Finland, Finland
Alfred Burian, University of Derby, United Kingdom
Dominik Martin-Creuzburg, Universität Konstanz, Germany
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