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Prostaglandins & other Lipid Mediators xxx (2013) xxx–xxx

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Prostaglandins and Other Lipid Mediators

1 Review

2 Production of EPA and DHA in aquatic ecosystems and their transfer to the land
3 Q1 Michail I. Gladyshev a,b,∗ , Nadezhda N. Sushchik a,b , Olesia N. Makhutova a
a
4 Institute of Biophysics of Siberian Branch of Russian Academy of Sciences, Akademgorodok, Krasnoyarsk 660036, Russia
b
5 Siberian Federal University, Svobodny av. 79, Krasnoyarsk 660041, Russia
6

7 a r t i c l e i n f o a b s t r a c t
8
9 Article history: Most omnivorous animals, including humans, have to some degree relied on physiologically important
10 Received 20 December 2012 polyunsaturated fatty acids (PUFAs), such as eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA)
11 Received in revised form 2 March 2013 from food. Only some taxa of microalgae, rather than higher plants can synthesize de novo high amounts of
12 Accepted 5 March 2013
EPA and DHA. Once synthesized by microalgae, PUFA are transferred through trophic chain to organisms
Available online xxx
of higher levels. Thus, aquatic ecosystems play the unique role in the Biosphere as the principal source
13
of EPA and DHA for most omnivorous animals, including inhabitants of terrestrial ecosystems. PUFA
14 Keywords:
are transferred from aquatic to terrestrial ecosystems through riparian predators, drift of carrion and
15 Eicosapentaenoic acid
16 Docosahexaenoic acid
seaweeds, emergence of amphibiotic insects, and water birds. The essential PUFA are transferred through
17 Aquatic ecosystems trophic chains with about twice higher efficiency than bulk carbon. Thereby, PUFA are accumulated,
18 Trophic transfer efficiency rather than diluted in biomass of organisms of higher trophic levels, e.g., in fish. Mankind is faced with a
severe deficiency of EPA and DHA in diet. Although additional sources of PUFA supply for humans, such
as aquaculture, biotechnology of microorganisms and transgenic terrestrial oil-seed producing plants
are developed, natural fish production of aquatic ecosystems will remain one of the main sources of EPA
and DHA for humans. Aquatic ecosystems have to be protected from anthropogenic impacts, such as
eutrophication, pollution and warming, which reduce PUFA production.
© 2013 Published by Elsevier Inc.

19 Contents

20 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
21 2. Production of EPA and DHA in natural ecosystems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
22 3. Export of aquatic PUFA to terrestrial ecosystems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
23 4. Transfer efficiency of the physiologically important PUFA through trophic chains . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
24 5. PUFA supply for humans . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
25 6. Protection of PUFA production in aquatic ecosystems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
26 7. PUFA content of various fish species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
27 8. Benefit vs. risk ratio of fish intake . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
28 9. PUFA content in cooked fish . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
29 10. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
30 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
31 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
32

36
33 1. Introduction
compounds of great physiological importance for animals at all tax- 37

onomic levels, including humans. EPA provides healthy functioning 38

34 In the past few decades long-chain polyunsaturated fatty acids
of cardiovascular system, and DHA is an important structural com- 39
35 of omega-3 family (PUFA), such as eicosapentaenoic acid, (EPA)
ponent of brain and retina, and also contributes to cardiovascular 40
and docosahexaenoic acid (DHA), have come to be recognized as
health [1–8]. However, animals, except the nematode Caenorhab- 41

ditis elegans, do not have special enzymes, 15/␻3 desaturases, to 42

insert double bound in the position ␻3 [9–11]. Only plants, algae, 43

Q2 ∗ Corresponding author at: Institute of Biophysics of Siberian Branch of Russian
photoautotrophic cyanobacteria, some heterotrophic protists and 44
Academy of Sciences, Akademgorodok, Krasnoyarsk 660036, Russia.
Tel.: +7 391 2494517; fax: +7 3912 433400. fungi, have 15 desaturases and can synthesize the parent acid of 45

E-mail addresses: glad@ibp.ru, michailgladyshev@yahoo.com (M.I. Gladyshev). ␻3 family, ␣-linolenic acid (18:3n-3, ALA) [12–14]. 46

1098-8823/$ – see front matter © 2013 Published by Elsevier Inc.

http://dx.doi.org/10.1016/j.prostaglandins.2013.03.002

Please cite this article in press as: Gladyshev MI, et al. Production of EPA and DHA in aquatic ecosystems and their transfer to the land.
Prostaglandins Other Lipid Mediat (2013), http://dx.doi.org/10.1016/j.prostaglandins.2013.03.002
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47 Thus, most animals can obtain the parent ␣-linolenic acid only Table 1
Content (mg g−1 C) of eicosapentaenoic and docosahexaenoic acids and their sum in
48 from food. In general, animals, including humans, can convert the
photoautotrophic and heterotrophic organisms, capable of their synthesis de novo.
49 parent ␣-linolenic acid to physiologically important long-chain EPA
50 and DHA [15]. Nevertheless, only around 5% of ALA is converted in Taxon 20:5n-3 22:6n-3 Sum Reference
51 long-chain PUFA in most studied omnivorous animals, including Microalgae
52 humans, and this route is unlikely to provide sufficient levels of Eustigmatophyceae
53 EPA and DHA for optimal human health [7,16]. Thereby, dietary Nannochloropsis limnetica 100.9 0.0 100.9 [21]
Cryptophyceae
54 intakes of the conditionally essential PUFAs, EPA and DHA, is of
Cryptomonas sp. 29.9 5.3 35.2 [21]
55 great importance for omnivorous animals. Rhodomonas lacustrisa 26.2 7.6 33.8 [22]
Rhodomonas lacustris 44.5 3.0 47.5 [23]
Rhodomonas salina 22.6 17.9 40.5 [24]
Rhodomonas salina 20.7 13.3 34.0 [25]
56 2. Production of EPA and DHA in natural ecosystems
Rhodomonas sp. 5.8 2.9 8.7 [26]
Bacillariophyceae (Diatomea)
57 Significant amounts of long-chain PUFA with 20–22 carbons, Chaetoceros calcitrans 20.6 2.1 22.7 [24]
58 EPA and DHA, can be synthesized by some algae, protists, fungi, Cyclotella meneghiniana 40.8 11.4 52.2 [27]
59 mosses and bacteria [9,17]. In contrast, terrestrial higher plants do Thalassiosira oceanica 45.9 7.5 53.4 [25]
Thalassiosira weissflogii 18.6 3.2 21.8 [26]
60 not have the ability to synthesize long-chain ␻-3 PUFAs such as EPA
Dinophyceae (Peridinea)
61 and DHA [17–20]. Gyrodinium dominans 11.1 38.4 49.5 [24]
62 Among primary producers in the Biosphere, microalgae, and, in Oxyrrhis marina 4.0 47.6 51.6 [24]
63 particular, diatoms, cryptophytes and dinophytes, can synthesize Prorocentrum dentatum 0.5 6.2 6.7 [26]
Peridiniopsis borgeia 8.3 11.7 20.0 [22]
64 high amounts of EPA and DHA per carbon unit of their biomass
Prymnesiophyceae
65 (Table 1). Algae synthesize more than half of the total primary Isochrysis galbana 3.7 22.1 25.8 [28]
66 production in Biosphere [42]. Terrestrial vascular plants give large Isochrysis galbana 8.1 27.0 35.1 [25]
67 amount of global primary production, but they don’t have EPA Phaeocystis globosab 1.7 4.9 6.6 [29]
68 and DHA. Thus, algae, both marine and freshwater, evidently are Prasinophyceae
Tetraselmis suecica 22.0 0.0 22.0 [24]
69 the main source of these two long-chain PUFA in the Biosphere
Macroalgae
70 (Table 2). Pheophyceae c

71 Besides microalgae, another marine microorganisms, thraus- Laminaria saccharina 1.7 0.0 1.7 [30]
72 tochytrids, can synthesize high amounts of EPA and DHA (Table 1). Laminaria digitata 1.5 0.0 1.5 [30]
Fucus vesiculosus 1.5 0.0 1.5 [30]
73 Thraustochytrids closely resemble zoosporic fungi in their mor-
Undaria pinnatifida 4.5 0.0 4.5 [30]
74 phology, but are classified in the phylum Heterokonta within the Halidrys siliquosa 0.5 0.0 0.5 [30]
75 kingdom Chromista, and no longer regarded as lower fungi [51,52]. Rhodophyceaed
76 Thraustochytrids are osmoheterotrophic and produce extracellular Porphyra umbilicalis 26.1 0.0 26.1 [30]
77 enzymes capable of breaking down several complex organic sub- Chondrus crispus 1.0 0.0 1.0 [30]
Palmaria palmata 13.4 0.1 13.6 [30]
78 strates [53]. They often accumulate up to 50% of their dry weight as
Gracilaria verrucosa 5.2 0.0 5.2 [30]
79 lipids, DHA frequently constituting 25% or more of these [54]. Most Water moss
80 part of DHA, ca. 95%, is primarily concentrated in TAG of thraus- Bryophyta
81 tochytrids [55]. Vegetative cells of thraustochytrids produce an Fontinalis antipyretica e 10.1 0.4 10.5 [31]
Arbuscular mycorrhizal fungi
82 extensive network of plasma membrane extensions, the ectoplas-
Glomeromycota
83 mic net elements (EN), when grown under nutrient poor conditions, Glomus spp. 6.0 0.0 6.0 [32]
84 the EN enabling them to take up nutrients from the surrounding Glomus irregularef 6.6 0.0 6.6 [33]
85 medium. The high accumulation of DHA in storage lipids of thraus- Saprotrophic fungi
86 tochytrids may be explained by the requirement of cells to form Zygomycota
Mortierella alpinaf 8.1 0.0 8.1 [34]
87 enormous amounts of membranes when the need arises to pro-
Thraustochytrids
88 duce the plasma membrane system of the EN [54]. Since ecological Labyrinthulomycetes g
[35]
89 role of thraustochytrids is decomposition of refractory organic sub- Aurantiochytrium sp. 5.4 86.4 91.7 [35]
90 strates in marine ecosystems (decaying fecal pellets of zooplankton, Schizochytrium sp. 7.8 30.0 37.8 [35]
91 algal tissue and mangrove leaves), their biomass in general is sig- Thraustochytrium sp. 14.7 56.6 71.3 [35]
Bacteria
92 nificantly lower, than that of planktonic microalgae [56]. Gamma Proteobacteria
93 The biosynthesis of EPA and/or DHA by bacteria (Table 1) Shewanella putrefaciensf 2.4 0.0 2.4 [36]
94 appears to be limited to a minority of deep-sea representatives, Shewanella gelidimarinaf 11.0 0.0 11.0 [37]
95 which thereby have a selective adaptation to temperature and/or a
Calculated from Tables 4 and 8 of the reference.
96 high pressure environments [37,57]. Contribution of these bacteria b
Calculated from Table 1 of the reference.
c
97 to the PUFA production in oceans is believed to be comparatively Calculated from the reference using C content 30% of dry weight (average from
98 negligible in global scale. [38–41]).
d
Calculated from the reference using C content 30% of dry weight (average from
99 Among terrestrial producers, only some species of soil algae and [41]).
100 lichens potentially may contribute to terrestrial autotrophic EPA e
Calculated from Table 1 and Fig. 1 of the reference, using C content 41% of dry
101 and DHA production, but there are no quantitative data on their weight (our unpublished data).
f
102 contribution to the PUFA supply, which may be regarded as negli- Calculated from the reference using C content 50% of dry weight [32].
g
Calculated from Table 2 of the reference as averages for groups of taxa from
103 gible in global scale. Indeed, algae may be comparatively abundant
Fig. 4.
104 in barren soil, but in vegetated soil they are evidently inhibited by
105 light deficiency due to plant cover [58].
106 In contrast to the terrestrial autotrophic organisms, some
107 species of soil heterotrophs, arbuscular mycorrhizal fungi (AMF) of
108 genus Glomus and saprotrophic fungi of genus Mortierella, can syn-
109 thesize de novo considerable amounts of EPA and/or DHA (Table 1).

Please cite this article in press as: Gladyshev MI, et al. Production of EPA and DHA in aquatic ecosystems and their transfer to the land.
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Table 2
Content of polyunsaturated fatty acids (PUFA, mg g−1 C), 20:5n-3 and 22:6n-3, in biomass of primary producers, average net primary production (NPP, g C m−2 y−1 ), global
biome area (GA, 1 × 106 km2 ), global NPP (GNPP , 1 × 1012 kg C y−1 ) and global PUFA production (GPUFA , 1 × 109 kg y−1 ).

Producer PUFA NPP [43] GA [43] GNPP GPUFA

Marine phytoplankton 7.0a 128 370.0 47.4 331.8

Marine macroalgae 6.2b 72 3.2 0.2 1.2
Freshwater phytoplankton 4.0c 290 23.4d 7.0e 28.0
a
Average value calculated from Table 2 of [44], Table 3 (open ocean) of [45], Table 2 of [46] and Table 2 of [47].
b
Average value calculated from Table 1 of this paper.
c
Average value calculated from Table 3 (estuary) of [45], Table 3 of [48] and Table 2 of [49].
d
Lakes and reservoirs 22.0 [50], estuaries 1.4 [43].
e
Lakes and reservoirs 6.8, estuaries 0.2.

110 However, at present there are no data to quantify production of in water. For instance, dragon flies, mosquitoes, non-biting midges 161

111 these PUFA by the fungi in various terrestrial ecosystems. More- and mayflies are amphibiotic insects. Their larvae feed on microal- 162

112 over, in contrast to aquatic microalgae, terrestrial fungi species, gae and other aquatic organisms, and when adult insects (imago) 163

113 capable of the synthesis of EPA and DHA, are not ubiquitous. For emerge from pupae and fly to the land, they bring in their bodies 164

114 instance, AMF are absent in boreal forests and in heathlands [59]. PUFA, synthesized by microalgae [69,70]. Adult amphibiotic insects 165

115 In some soil ecosystems there may be a peculiar source of EPA are consumed by various terrestrial animals (Fig. 1). It is important 166

116 and DHA. For instance, earthworms Lumbricus terrestris had com- to emphasize, that in contrast to the amphibiotic insects, most ter- 167

117 paratively very high concentrations of PUFA in their body tissues, restrial insects contain no or negligible amounts of EPA and DHA 168

118 which originated from their gut microorganisms rather than bulk (e.g., [71,72]). The global export of EPA plus DHA through insect 169

119 soil [60]. Thus, gut microbiota may be a source of the long-chain emergence was estimated to be around 240 × 106 kg y−1 (Fig. 1), 170

120 PUFA for some detritivorous soil organisms like earthworms and i.e., two orders of magnitude higher, that that of riparian predators. 171

121 Collembola [60]. Besides, as mentioned above, the nematode C. Water birds also are the important conduit of the EPA and 172

122 elegans can synthesize EPA de novo [12–14,61]. However, these ter- DHA from aquatic to terrestrial ecosystems (Fig. 1). They con- 173

123 restrial sources of PUFA are not quantified yet. In general, they are sume aquatic prey, zooplankton, zoobenthos and fish, and in turn, 174

124 believed to be globally negligible compared to the production of the birds and their eggs are consumed by terrestrial predators. 175

125 aquatic algae. Indeed, in many soil samples taken around the world Global PUFA export through water birds was estimated to be about 176

126 EPA and DHA were not detected at all (e.g., [62–64]). 432 × 106 kg y−1 (Fig. 1). 177

127 As mentioned above, animals can convert ALA to EPA and DHA Another way of the PUFA export, occurred primarily in oceans, 178

128 [15]. Evidently, strictly herbivorous terrestrial animals, such as is a shore drift of carrion and seaweeds. The EPA and DHA export 179

129 grazing mammals, consuming vascular plants, must rely on the via the drift was estimated to be around 24 × 106 kg y−1 (Fig. 1). 180

130 conversion only. Thereby, they seem to satisfy only their own phys- Thus, total global natural export of EPA and DHA from aquatic 181

131 iological requirements in the long chain PUFA, but hardly can be to terrestrial ecosystems is ca. 698 × 106 kg y−1 (Fig. 1). Using data 182

132 a considerable source of EPA and DHA for carnivorous animals. from Table 2, we can calculate that the export is only 0.2% of total 183

133 Indeed, contents of these PUFA in biomass of herbivorous mam- production of EPA and DHA in aquatic ecosystems, 361 × 109 kg y−1 . 184

134 mals appeared to be very low (Table 3), especially compared to

135 those of fish (see below in Chapter 7). It should be noted that we
4. Transfer efficiency of the physiologically important 185
136 failed to find quantitative data on EPA and DHA content in biomass
PUFA through trophic chains 186
137 of wild animals, such as deer, elk, hare, etc., in ISI Web of Knowl-
138 edge (version 5.7), and in all publications only per cent levels of
PUFA are transferred from aquatic to terrestrial ecosystems 187
139 these fatty acids in total FAs were given. Thus, we have to rely on
through comparatively long trophic chains, which include both 188
140 data on domestic animals, fed on plant food, rich in ALA (Table 3).
aquatic and terrestrial organisms. It is important to note, that one of 189
141 Consequently, terrestrial sources of EPA and DHA at present
the central paradigms of ecology (the concept of trophic pyramid) 190
142 appeared to be minor contributors, although variations in PUFA
is that only about 10% of energy-yielding compounds of carbon, 191
143 supply in different ecosystems seem to be considerable. There-
produced at one trophic level, are incorporated into new biomass 192
144 fore, in general aquatic ecosystems are regarded to play the special
of organisms of the next trophic level [73]. In other words, trans- 193
145 role in the Biosphere as the principal source of the long-chain ␻-
fer efficiency of organic carbon (energy) between trophic levels is 194
146 3 PUFA for many omnivorous and carnivorous animals, including
about 10%. The question arises: how can a considerable amount 195
147 inhabitants of terrestrial ecosystems [50].
of the essential PUFA, synthesized by microalgae, reach terrestrial 196

consumers, if the concept of trophic pyramid is true for them and 197

148 3. Export of aquatic PUFA to terrestrial ecosystems PUFA losses in trophic chains are about 90% at each step? 198

To answer this question we studied trophic transfer efficiency 199

149 Once synthesized at the level of primary producers, algae, EPA (TTE) between primary producers (phytoplankton) and consumers 200

150 and DHA are transferred through trophic chains to organisms (zooplankton) of bulk carbon vs. the essential ␻3-PUFA [74]. For 201

151 of progressively higher trophic levels, including terrestrial con- a comparison we also calculated TTE of non-essential C16-PUFA. 202

152 sumers. There are several main ways of export of production of These acids are synthesized exclusively by microalgae, and ani- 203

153 aquatic ecosystems, including PUFA, to terrestrial ecosystems [50] mals can use them for mitochondrial ␤-oxidation only, that is 204

154 (Fig. 1). The first way is a direct consumption of aquatic prey by to obtain energy. This approach was novel, because all previous 205

155 riparian predators. The export of aquatic PUFA to terrestrial preda- studies have looked at the transfer efficiency of bulk carbon with- 206

156 tors, bears, consumed spawning salmon, was estimated in the place out distinguishing between different types of carbon compounds. 207

157 of their highest activity, in the Pacific Rim, and was found to be Trophic transfer efficiency was defined by conventional mean, as 208

158 2 × 106 kg of EPA + DHA per year in global scale (Fig. 1). ratio between secondary production of zooplankton and primary 209

159 Another way of the PUFA export is emergence of amphibiotic production of phytoplankton. Average trophic transfer efficiency of 210

160 insects [50]. Larvae and pupae of these insects grow and develop PUFA, 9.3 ± 2.7%, was significantly higher, than that of bulk carbon, 211

Please cite this article in press as: Gladyshev MI, et al. Production of EPA and DHA in aquatic ecosystems and their transfer to the land.
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Table 3
Content of eicosapentaenoic and docosahexaenoic acids (g kg−1 , wet weight) in muscle tissues of mammals, ranged by EPA + DHA content values.

Animals EPA DHA EPA + DHA Source

Sheep 0.18 0.07 0.25 [65] (sum from Tables 3 and 4 of the source, basal diet)
Pigs 0.11 0.04 0.15 [66] (mean from Table 5 of the source)
Rabbits 0.04 0.04 0.08 [67] (mean from Table 5 of the source)
Cattle 0.05 0.02 0.07 [68] (Table 5 of the source, control)

212 4.8 ± 1.3%. In contrast, TTE value of the non-essential C16-PUFA, by emerging insects (Fig. 1). Average biomass of these deer mice in 243

213 3.3 ± 0.2%, on average was lower, than those of bulk C [74]. diverse ecosystems ranges between 1.7 and 29.9 kg km−2 , and their 244

214 Lipids are known to have energy of complete oxidation sig- EPA + DHA requirements were estimated accordingly to be from 245

215 nificantly higher, than that for the same weight of other carbon 0.37 kg km−2 y−1 to 6.53 kg km−2 y−1 [50]. The supply of these PUFA 246

216 compounds, carbohydrates or proteins. Such lipids as the C16-PUFA per unit of terrestrial area due to emerging insects was calculated to 247

217 seemed to be preferentially oxidized by the animals compare to be from 2.5 to 11.8 kg km−2 y−1 [50]. Thus, in general the supply of 248

218 other carbon compounds. In contrast, zooplankton do not respire EPA and DHA from aquatic ecosystems meets requirements of the 249

219 ␻3-PUFAs, but rather store them [74]. most abundant terrestrial omnivorous animals, but there may also 250

220 It is worth to note, that regarding the above finding for zoo- be a shortage of PUFA in rodent populations. It should be noted 251

221 plankton [74] an analogy with human organism may be drawn. As that strictly herbivorous terrestrial animals, as mentioned above, 252

222 reported by some authors [5,75], 50–70% of oral doses of short- evidently obtain EPA and DHA synthesizing them from ALA (see 253

223 chain PUFA are oxidized (used for energy) in 24 h. In comparison, Chapter 2 and Table 3). 254

224 DHA is selectively incorporated into cell membranes, with only 15%
225 is oxidized [5,75].
226 Thus, now we can see, that the essential PUFA are transferred 5. PUFA supply for humans 255
227 through trophic chains at about twice higher efficiency, than bulk
228 carbon and thereby they are bioaccumulated, rather than diluted, in Besides natural fluxes, there is an anthropogenic export of PUFA 256
229 biomass of organisms of higher trophic level, namely in zooplank- from aquatic ecosystems, i.e., human fishery (Fig. 1). The anthro- 257
230 ton [74]. The bioaccumulation of PUFA in aquatic trophic chains pogenic export was calculated using data on total world catch and 258
231 also appeared to be a characteristic of an aquatic-terrestrial trophic using a generalization on average EPA + DHA content in fish and 259
232 chain. When comparing EPA and DHA content in biomass of fish and invertebrates, 2 mg g−1 of wet weight (WW). As found, man with- 260
233 their terrestrial consumers, gray herons, it was found that contents draws from aquatic ecosystems about 180 million kg of EPA and 261
234 of these PUFA in muscle tissue of herons were about twice higher, DHA per year [50]. This value is lower, than those for water birds 262
235 than in those of the fish [76]. and emerging aquatic insects, but significantly higher, than that for 263
236 Another important question is: can PUFA export from aquatic riparian predators (Fig. 1). 264
237 ecosystems meet the PUFA requirements of omnivorous terrestrial Human consumption of wild and farmed fish and aquatic inver- 265
238 animals? To answer this question, data on omnivorous rodents, tebrates is ∼16 kg per person per year. This means that the global 266
239 deer mouse (Peromyscus maniculatus), were generalized. Rodents average personal daily consumption of EPA + DHA is about 0.1 g 267
240 are known to have the highest population biomass among all other [50]. International recommendations for personal intakes to reduce 268
241 terrestrial vertebrates. Since deer mice also consume insects, their risk for cardiovascular diseases and psychiatric disorders are of 269
242 PUFA requirements were compared with the export of EPA and DHA ∼0.5–1 g of EPA + DHA per day [2,77–79]. Thus, mankind is faced 270

Fig. 1. Ways of export of eicosapentaenoic and docosahexaenoic acids from aquatic to terrestrial ecosystems: figures in squares are global estimations of quantity of exported
EPA + DHA [50].

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271 with a deficiency of the physiologically important long-chain PUFA of this process, considering, for instance, a dismal fail of production 337

272 in diet. of cocoa butter substitutes by yeasts in the 1980s [19]. In any case, 338

273 Worldwide exploitation rates of fisheries have been shown at present, the contribution of microbial PUFAs to the oil industry 339

274 to be too high, even at present and cannot be higher than is nearly negligible [82,86]. High cost of SCO restricts their use to 340

275 100 × 106 metric tons per year [80]. There are three potential ways infant formulae and medical foods and generally prohibits their 341

276 to increase PUFA supply: (1) aquaculture; (2) biotechnology of inclusion in common food products [87]. 342

277 microorganisms and 3) genetic engineering, i.e., insertion of genes The third potential way to increase the long-chain PUFA sup- 343

278 directing PUFA synthesis into terrestrial oil-seed producing plants. ply is a production of transgenic plant oil. Several sets of genes 344

279 Aquaculture at present gives about 70 × 106 tons of fish and encoding enzymes in alternative biosynthetic pathways have been 345

280 invertebrates per year, i.e., it approaches the total world catch [81]. isolated from a number of marine microalgae, thraustochytrids, 346

281 However, there are two potential limitations of increase of aqua- and terrestrial fungi and transferred to several different plants [88]. 347

282 culture production. Firstly, sections of natural water bodies, seas, Although the introduction of EPA and DHA biosynthetic pathways 348

283 lakes and rivers are used for aquaculture, and thereby aquacul- into oilseed crops has been successfully demonstrated, reaching 349

284 ture provides substantial pollution of these natural water bodies economically viable levels of EPA and DHA has proved challenging 350

285 [81]. Pollution provides a negative impact on wild fish populations, [20,87]. 351

286 which still is the main source of PUFA for humans. Secondly, fish
287 reared in aquaculture, required for their development and growth
288 PUFA-rich feed. The principal source of PUFA rich feed for aqua- 6. Protection of PUFA production in aquatic ecosystems 352

289 culture is wild catch of fish and invertebrates, which cannot be

290 increased. For instance, 70% of fish oil production at present is uti- Thus, in spite of development of aquaculture, microbial pro- 353

291 lized for the production of fish feed for farmed fish [82]. Salmon duction processes and the genetic engineering for vascular oilseed 354

292 aquaculture use up much more fish flesh than they produce, and plants, natural fish production of aquatic ecosystems will remain 355

293 hence cannot replace capture fisheries [80]. one of the main sources of the conditionally essential PUFA, EPA 356

294 Microorganisms, including genetically modified strains, are and DHA, for most humans [86]. Thereby, protection of aquatic 357

295 believed to be a reliable, economically attractive source for large- ecosystems to support high levels of natural fish production is the 358

296 scale production of the long-chain PUFA in the near future [57]. essential challenge for mankind. 359

297 Among microorganisms, bacteria are probably not suitable as PUFA It is important to note that aquatic ecosystems naturally dif- 360

298 producers, as they do not accumulate triacylglycerols [82]. Pho- fer in their ability to produce PUFA. As mentioned above, only 361

299 toautotrophic microalgae, which are the main producers of EPA some microalgae taxa, diatoms, cryptophytes, dinophytes, etc., can 362

300 and DHA in nature (Tables 1 and 2), do not play the principal role in synthesize EPA and DHA (Table 1). Other algal taxa, such as Chloro- 363

301 the biotechnological production of these acids. Even with techno- phyceae, as well as cyanobacteria (blue-green algae) don’t produce 364

302 logically advanced bioreactors for algal fermentations, maximum EPA and DHA [89–91]. However, lakes and reservoirs are often dom- 365

303 densities attained are low due to unsolved problems (e.g., light inated namely by cyanobacteria and Chlorophyceae. Domination 366

304 limitation and oxygen accumulation), making such processes cost- or “blooming” of cyanobacteria is favored by anthropogenically- 367

305 prohibitive for production of industrial products [19,82,83]. Thus, induced eutrophication, i.e., increase of phosphorus load in natural 368

306 numerous EPA and DHA-producing microalgae (Isochrysis, Chaeto- water bodies. Thus, to support the natural production of EPA and 369

307 ceros, Nannochloropsis, Phaeodactylum and Pavlova) are cultivated DHA in lakes and reservoirs, they must be prevented from the 370

308 in the aquaculture industry at relatively low cell densities, mainly eutrophication. To prevent eutrophication and to restore “bloom- 371

309 for the enrichment of zooplankton and fish juvenile stages [19,84]. ing” lake, special measures must be taken: (1) decrease of external 372

310 Alternatively, large-scale production of algal fatty acids is pos- phosphorus load by waste water treatment; (2) decrease of internal 373

311 sible through the use of heterotrophic microalgae growing on phosphorus load by dredging of bottom sediments and/or aeration 374

312 reduced carbon sources in fermentation systems which provide of anaerobic near-bottom water layer (hypolimnion); (3) bioma- 375

313 consistent biomass under highly controlled conditions result- nipulation by trophic chains to increase abundance of piscivorous 376

314 ing in a very high quality product [82,83]. Using an obligatory fish and macrophytes which inhibit cyanobacteria by a number of 377

315 heterotrophic marine dinoflagellate microalgae Crypthecodinium indirect and direct ecological effects [92]. 378

316 cohnii, DHA productivities of 1–1.5 g L−1 day−1 are achievable [19]. Anthropogenic pollution of aquatic ecosystems by heavy metals, 379

317 C. cohnii is used for industrial production of single cell oil (SCO), con- petroleum products, etc., also can decrease PUFA production. For 380

318 taining DHA, which is currently applied mainly for fortification of instance, pollution by Cu, Pb, and Cd caused a decrease of efficiency 381

319 infant formulae and for dietary supplements in the form of gelatine of transfer of EPA and DHA through a trophic chain of a river ecosys- 382

320 capsules [19,82]. tem and decrease of contents of these PUFA in biomass of organisms 383

321 Regarding volumetric productivity, the best microbial sources of of upper trophic levels, including fish [93]. Besides, the pollution by 384

322 DHA are strains of thraustochytrid species of genus Schizochytrium, heavy metals and toxic organic compounds deteriorates nutritive 385

323 which have DHA productivities of ∼10 g L−1 day−1 [19]. However, quality of fish production in spite of any PUFA content (see Section 386

324 for infant formulae, which constitute the major market for DHA, 8). Evidently, prevention of any anthropogenic pollution of aquatic 387

325 this fatty acid coming from C. cohnii, rather than Schizochytrium ecosystems is necessary to support both quantity and quality of 388

326 [85]. In turn, Schizochytrium-derived DHA is finding use in adult catches. 389

327 food supplements, and is applied as feed to broiler chickens and Another threat to the PUFA production is climate warming. PUFA 390

328 laying hens feed in order to enhance DHA in the meat and eggs synthesis by microalgae is known to inversely depend on tem- 391

329 [85]. Schizochytrium also has been used in aquaculture to signifi- perature. At higher temperatures algae decrease the proportion of 392

330 cantly enrich DHA levels of rotifers and Artemia larvae before they low-melting PUFA in their lipids to maintain proper cell membrane 393

331 are fed to larval fish and shrimp [19,85]. In contrast to DHA, EPA fluidity [42]. 394

332 productivities have remained low in commercial terms. Culture Evidently, a decrease of PUFA synthesis by microalgae results in 395

333 with the heterotrophic diatom Nitzschia laevis have the highest EPA concomitant decrease of PUFA content in following links of trophic 396

334 productivities of 0.175 g L−1 day−1 only [19]. chain, zooplankton and fish larvae, which primarily feed on zoo- 397

335 Although SCO are now widely accepted in the market place, one plankton. For instance, in warm lakes content of EPA and especially 398

336 should be cautious about predicting the future commercial success DHA in zooplankton, was found to be significantly lower, than that 399

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400 in cold lakes [49]. In zooplankton of cold lakes copepods were the Victoria and Kyoga, food fish species, tilapia, perch (order Per- 463

401 dominant taxa [49]. Copepods are rich in DHA [94], which is essen- ciformes), squeaker, catfish (order Siluriformes), lungfish (order 464

402 tial for growth and development of fish larvae [95]. Thereby fish Lepidosireniformes) (Table 4), are so lean that it will be impossible 465

403 larvae, which feed on copepods, have a high content of this essen- to cover the daily recommended intake of 500 mg of EPA + DHA by 466

404 tial PUFA in their diet. In contrast to cold lakes, in warm lakes the eating these fish alone [108]. However, it is worth to note, that there 467

405 dominant zooplankton taxa were cladocerans, which are poor in may be a large variation of PUFA content in same fish species from 468

406 DHA [49]. Thus, fish in warm lakes seem to have comparatively different water bodies. For instance, in Ethiopian lakes EPA + DHA 469

407 lower PUFA supply. Indeed, in European lakes climate warming in contents of Nile tilapia (Oreochromis niloticus) varied from 3.09 to 470

408 conjunction with eutrophication stimulates a shift from salmonid 13.21 mg g−1 of dry weight ([116], calculated from Table V of the 471

409 fish to cyprinid fish [96]. This shift in fish species composition is reference). Using average moisture content of Nile tilapia 77.9% 472

410 believed to be crucial for EPA and DHA catch, because various fish ([117], calculated from Table 3 of the reference), we can get PUFA 473

411 taxa dramatically differ in EPA and DHA content in their biomass. content range 0.7–2.9 g kg−1 of wet weight, i.e., the upper value 474

is ca.4 times higher, than the lower one, given for this species in 475

Table 4. Thus, continual improvement of databases on PUFA con- 476

412 7. PUFA content of various fish species tent of food fish, especially freshwater fish in different areas of 477

the world, is crucial in order to compare the benefits they offer 478

413 Contemporary data set on EPA and DHA content in many fish for consumer health [79,113]. Thereby, global inventory of aquatic 479

414 species (Table 4) allows making some generalizations. Marine fish ecosystems concerning their ability to produce PUFA and transfer 480

415 species, such as sardine and herring (order Clupeiformes), have the them through trophic chains to fish is very desirable. 481

416 highest EPA + DHA contents, reported for wild fish in the available
417 literature (Table 4). These fish species are pelagic and zooplank- 8. Benefit vs. risk ratio of fish intake 482
418 tivorous, i.e., they inhabit water column and fed on zooplankton,
419 copepods, which as mentioned above (Section 6), have very high As mentioned above (Section 6), nutritive quality of fish in spite 483
420 content of EPA and DHA in their lipids. Marine pelagic copepods are of any PUFA content can be diminished by anthropogenic pollu- 484
421 especially rich in lipids, which compose up to 75% of their dry mass tion. Besides the essential nutrients, PUFA, toxic materials, such 485
422 [112]. The maximum reported value of EPA + DHA for wild fresh- as heavy metals, pesticides and radionuclides can be transferred 486
423 water fish, brown trout (order Salmoniformes), is only 4.4 g kg−1 of through aquatic trophic chains and accumulated in organisms of 487
424 wet weight (Table 4). Some authors suggested that consumption of higher trophic levels, namely in fish [118–121]. 488
425 freshwater fish did not provide health benefits compared to that of Different fish species from diverse locations have different con- 489
426 marine fish [113]. However, minimum reported value of EPA + DHA tents of PUFA (Table 4), as well as different concentrations of toxic 490
427 content for marine species, garfish (order Beloniformes), is only compounds. Thus, a quantitative estimation of risks versus benefits 491
428 0.2 g kg−1 , while the minimum known value for freshwater species, of fish intake for human health is very important. Such estimation 492
429 marbled lungfish (order Lepidosireniformes), is 0.4 g kg−1 (Table 4). could allow people to make informed decisions about which fish to 493
430 Thus, there is a considerable overlap of ranges of the PUFA con- eat to reduce their risk from the contaminants and increase health 494
431 tents of marine (25.6–0.2 g kg– 1) and freshwater (4.4–0.4 g kg−1 ) benefits. A ratio between benefit and risk for intake of food fish 495
432 fish. It is worth to remark, that besides the differences in EPA + DHA contained the conditionally essential PUFA vs. heavy metals can be 496
433 contents, various fish species also have different EPA:DHA ratios quantified by a dimensionless hazard quotient, HQPUFA :
497

434 (Table 4). Although current recommendations for personal intakes

435 regard sum of these PUFA [2,77–79], EPA and DHA evidently play REFA c
HQPUFA = , 498
436 different roles in human organism (see Section 1). Thus, a consid- C · RfD · AW
437 eration of probable influence of EPA:DHA ratio on nutritive values
438 of diverse fish species seems to be an important future task. where REFA (mg day−1 ) is the recommended daily dose of EPA + DHA 499

439 At present it is not known, if PUFA content of fish is con- for a human person; small c (␮g g−1 ) is content of a given metal in 500

440 trolled by phylogenetic or ecological and trophic factors. For aquatic a given fish; capital C (mg g−1 ) is content of PUFA in a given fish; 501

441 invertebrates a growing body of evidence suggests that namely RfD (␮g kg−1 day−1 ) is a reference dose, defined as the maximum 502

442 phylogenetic factors are primarily determinants of their fatty acid tolerable daily intake of a specific metal that does not result in any 503

443 composition [114,115]. More work should be done for fish. For deleterious health effects and AW (kg) is an average adult weight 504

444 instance, two forms of the same species, Oncorhynchus nerka (order [122]. HQEFA value less than 1 means the health benefit from fish 505

445 Salmoniformes), from lakes in Kamchatka Peninsula (Russia) were consumption, and HQEFA value higher than 1 means the risk for 506

446 compared [105]. One form, sockeye salmon was anadromous, that health. To prevent people from deleterious effect of fish consump- 507

447 is, juvenile fish migrate in ocean to feed and grow. The other form, tion and to provide healthy diets, a regular monitoring of the hazard 508

448 named kokanee, was landlocked and lived in a lake. Although the quotients for food fish in wild conditions based at least on monthly 509

449 sockeye salmon was found to have slightly higher content of EPA sampling frequency is required [122]. 510

450 and DHA, than the kokanee (Table 4), these differences were not
451 statistically significant [105]. This means, that PUFA level in the 9. PUFA content in cooked fish 511

452 fish may be controlled primarily by phylogenetic factors. Environ-

453 mental factors seem to control PUFA stock in an aquatic ecosystem All the above data on PUFA content in diverse fish species were 512

454 indirectly, through changing of species composition. For instance, based on analyses of raw fish. However, the consumption of raw 513

455 as mentioned above (Section 6), in European lakes climate warming fish is rare in Western society, and information about PUFA con- 514

456 caused a shift from salmonids (order Salmoniformes), which fresh- tents of raw fish may have limited significance for a conclusion on 515

457 water species contain more than 2 g kg−1 of EPA + DHA, to cyprinids their nutritive value [123]. Fish products are prepared by heating 516

458 (order Cypriniformes), which contain only around 1 g kg−1 of these and other culinary treatments. The problem is that the long-chain 517

459 PUFA (Table 4). PUFAs are considered to be highly susceptible to oxidation, and 518

460 In any case, in different ecosystems various fish species have an exposure to high temperature treatment may cause deterio- 519

461 very different PUFA content and thereby they considerably differ ration of these fatty acids in foods [124,125]. Indeed, pure PUFA 520

462 in their nutritive value for humans. For instance, in African lakes are easily degraded under heating. Nevertheless, in fish PUFA are 521

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Table 4
Content of eicosapentaenoic and docosahexaenoic acids (g kg−1 , wet weight) in various wild fish species. Orders and species are ranged by EPA + DHA content values.

Species EPA DHA EPA + DHA Source

Order Clupeiformes
Sardine (Sardinops sagax) 6.6 19.0 25.6 [97]
Herring (Clupea harengus) 8.5 8.3 16.8 [97]
Shad (Alosa alosa) 0.12 0.43 0.5 [98]
Order Salmoniformes
Atlantic salmon (Salmo salar) 6.2 5.8 12.0 [99]
Pink salmon (Oncorhynchus gorbuscha) 1.7 3.3 5.0 [100]
Brown trout (Salmo trutta)a 0.9 3.5 4.4 [101]
Arctic charr Salvelinus alpinesa 1.3 2.8 4.1 [101]
Rainbow trout (Oncorhynchus mykiss)a 0.9 3.1 4.0 [101]
Whitefish (Coregonus clupeaformis)a 0.7 2.4 3.1 [102]
European grayling (Thymallus thymallus)b 0.9 2.0 2.9 [103]
Siberian grayling (Thymallus arcticus) 0.7 1.9 2.6 [104]
Sockeye salmon (Oncorhynchus nerka) 0.7 1.9 2.6 [105]
Kokanee salmon (Oncorhynchus nerka) 0.6 1.5 2.1 [105]
Order Osmeriformes
Surf smelt (Hypomesus pretiosus) 3.6 5.7 9.3 [97]
Capelin (Mallotus villosus) 3.6 4.6 8.2 [97]
Order Scorpaeniformes
Canary rock fish (Sebastes pinniger) 3.5 5.4 7.9 [97]
Scorpion (Scorpaena scrofa) 0.29 1.4 1.7 [98]
Order Perciformes
Horse mackerel (Trachurus trachurus) 1.64 5.86 7.5 [98]
Black scabbard fish (Aphanopus carbo) 0.8 2.9 3.7 [106]
White sea bream (Diplodus sargus) 1.0 2.3 3.3 [107]
Gilthead sea bream (Sparus aurata) 0.9 2.0 2.9 [107]
Sea bass (Dicentrarchus labrax) 0.52 1.75 2.3 [98]
Red mullet (Mullus barbatus) 0.48 0.94 1.9 [98]
Perch (Perca fluviatilis)b 0.3 0.9 1.2 [103]
Ruffe (Gymnocephalus cernuus)b 0.4 0.8 1.2 [103]
Zander (Lucioperca lucioperca)b 0.2 0.8 1.1 [103]
Redbelly tilapia (Tilapia zilli) 0.1 0.5 0.7 [108]
Nile tilapia (Oreochromis niloticus) 0.1 0.6 0.7 [108]
Nile perch (Lates niloticus) 0.1 0.5 0.6 [108]
Brown meager (Sciaena umbra) 0.05 0.19 0.2 [98]
Bonito (Sarda sarda) 0.03 0.15 0.2 [98]
Order Anguilliformes
European eel (Anguilla anguilla)b 1.6 2.2 3.7 [103]
Order Gadiformes
Alaska pollock (Theragra chalcogramma) 1.0 2.4 3.4 [97]
Pacific hake (Merluccius productus) 0.9 1.5 2.4 [97]
Cod (Gadus morhua) 0.6 1.5 2.1 [109]
Burbot (Lota lota)b 0.5 0.9 1.3 [103]
Whiting (Gadus merlangus) 0.08 0.48 0.6 [98]
Order Pleuronectiformes
Rock sole (Lepidopsetta bilineata) 1.8 1.1 2.9 [109]
Order Cypriniformes
Ide (Leuciscus idus)b 0.5 1.1 1.6 [103]
Gibel carp (Carassius gibelio) 0.6 1.0 1.6 [110]
Roach (Rutilus rutilus)b 0.4 1.0 1.4 [103]
White bream (Blicca bjoerkna)b 0.4 0.8 1.2 [103]
Bream (Abramis brama)b 0.4 0.6 1.0 [103]
Tench (Tinca tinca)b 0.3 0.5 0.8 [103]
Crucian carp (Carassius carassius)b 0.2 0.6 0.8 [103]
Silver bream (Blicca bjoerkna) 0.2 0.5 0.7 [76]
Order Esociformes
Pike (Esox lucius)b 0.3 1.0 1.3 [103]
Order Siluriformes
Lake Victoria squeaker (Synodontis victoriae) 0.2 0.7 0.9 [108]
Sudan catfish (Bagrus docmas) 0.1 0.7 0.8 [108]
African sharptooth catfish (Clarias gariepinus) 0.2 0.5 0.7 [108]
Order Mugiliformes
Mullet (Mugil cephalus) 0.46 0.08 0.5 [98]
Order Lepidosireniformes
Marbled lungfish (Protopterus aethiopicus) 0.1 0.3 0.4 [108]
Order Beloniformes
Garfish (Belone belone) 0.01 0.15 0.2 [98]
a
The data were recalculated from dry weight using average moisture content in Salmoniformes 72.5% [100,104,109,111].
b
The data were recalculated from mg g−1 of dry weight (DW) to g kg−1 of wet weight (WW) using DW/WW (%) ratios given in Table 1 of the reference.

522 contained in phospholipids of cell membranes, where they are and DHA did not decrease under various ways of cooking compared 526

523 closely packed and surrounded with proteins. Thereby, their sus- to raw fish [100,109,126]. 527

524 ceptibility to degradation by heating may differ from that of pure In Table 5 data on EPA + DHA content in some products from 528

525 PUFA. Really, as found for many fish species, their content of EPA available literature are summarized and ranged. Like in raw fish, 529

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Table 5 [3] SanGiovanni JP, Chew EY. The role of omega-3 long-chain polyunsatu- 568
The quantity of products to be consumed for obtaining the recommended appropri- rated fatty acids in health and disease of the retina. Prog Retin Eye Res 569
ate intake of sum of eicosapentaenoic and docosahexaenoic fatty acids for humans, 2005;24:87–138. 570
1 g day−1 . [4] McNamara RK, Carlson SE. Role of omega-3 fatty acids in brain development 571
and function: potential implications for the pathogenesis and prevention of 572
Product Quantity (g) Reference psychopathology. Prostaglandins Leukot Essent Fatty Acids 2006;75:329–49. 573
[5] Plourde M, Cunnane SC. Extremely limited synthesis of long chain polyun- 574
Pacific saury (canned) 41 [126]
saturates in adults: implications for their dietary essentiality and use as 575
Atlantic salmon (fried) 51 [127]
supplements. Appl Physiol Nutr Metab 2007;32:619–34. 576
Pacific herring (canned) 56 [126] [6] Bazan NG. Cellular and molecular events mediated by docosahexaenoic acid- 577
Baltic sprat (canned) 70 [126] derived neuroprotectin D1 signaling in photoreceptor cell survival and brain 578
Humpback salmon (boiled) 167 [100] protection. Prostaglandins Leukot Essent Fatty Acids 2009;81:205–11. 579
Brown trout (boiled) 175 [109] [7] Wall R, Ross RP, Fitzgerald GF, Stanton C. Fatty acids from fish: the 580
Humpback salmon (stewed) 189 [100] anti-inflammatory potential of long-chain omega-3 fatty acids. Nutr Rev 581
Humpback salmon (roasted) 200 [100] 2010;68:280–9. 582
Humpback salmon (fried) 233 [100] [8] Phang M, Lazarus S, Wood LG, Garg M. Diet and thrombosis risk: nutrients for 583
Brown trout (fried) 244 [109] prevention of thrombotic disease. Semin Thromb Hemost 2011;37:199–208. 584
Cod (fried) 246 [127] [9] Uttaro AD. Biosynthesis of polyunsaturated fatty acids in lower eukaryotes. 585

Herring (boiled) 256 [109] IUBMB Life 2006;58:563–71. 586

Herring (fried) 263 [109] [10] Lands WEM. Human life: caught in the food web. In: Arts MT, Kainz M, 587
Brett MT, editors. Lipids in aquatic ecosystems. New York: Springer; 2009. 588
Rock sole (boiled) 278 [109]
p. 327–54. 589
Rock sole (fried) 323 [109]
[11] Zhou X-R, Green AG, Singh SP. Caenorhabditis elegans 12-desaturase FAT-2 590
Cod (boiled) 417 [109]
is a bifunctional desaturase able to desaturate a diverse range of fatty acid 591
Prawn (fried) 563 [128] substrates at the 12 and 15 positions. J Biol Chem 2011;286:43644–50. 592
Pork (pan-fried) 3333 [129] [12] Sperling P, Ternes P, Zank TK, Heinz E. The evolution of desaturases. 593
Prostaglandins Leukot Essent Fatty Acids 2003;68:73–95. 594
[13] Sayanova O, Haslam R, Guschina I, et al. A bifunctional 12, 15-desaturase 595
from Acanthamoeba castellanii directs the synthesis of highly unusual n-1 596
530 the nutritive value of different cooked fish species differed in about series unsaturated fatty acids. J Biol Chem 2006;281:36533–41. 597
531 ten times. Surprisingly, canned fish appeared to be more valuable [14] Alloatti A, Uttaro AD. Highly specific methyl-end fatty-acid desaturases of 598

532 products concerning the PUFA content. To get the recommended trypanosomatids. Mol Biochem Parasitol 2011;175:126–32. 599
[15] Stark AH, Crawford MA, Reifen R. Update on alpha-linolenic acid. Nutr Rev 600
533 daily dose, one needs to eat only 40 g of canned saury (Table 5). It is 2008;66:326–32. 601
534 important to emphasize that in terrestrial animal products contents [16] Davis BC, Kris-Etherton PM. Achieving optimal essential fatty acid status in 602

535 of EPA and DHA are at least ten times lower than those in fish. For vegetarians: current knowledge and practical implications. Am J Clin Nutr 603
2003;78(Suppl.), 640S–6S. 604
536 instance, to get 1 g of EPA + DHA, one needs to eat more than 3 kg [17] Sayanova OV, Napier JA. Eicosapentaenoic acid: biosynthetic routes and the 605
537 of pan-fried pork (Table 4). potential for synthesis in transgenic plants. Phytochemistry 2004;65:147–58. 606
[18] Harwood JL. Recent advances in the biosynthesis of plant fatty acids. Biochim 607
Biophys Acta 1996;1301:7–56. 608
538 10. Conclusions [19] Ward OP, Singh A. Omega-3/6 fatty acids: alternative sources of production. 609
Process Biochem 2005;40:3627–52. 610
[20] Ruiz-Lopez N, Sayanova O, Napier JA, Haslam RP. Metabolic engineering of 611
539 Aquatic ecosystems appeared to be the important producers the omega-3 long chain polyunsaturated fatty acid biosynthetic pathway into 612
540 and providers of EPA and DHA for many omnivorous terrestrial transgenic plants. J Exp Bot 2012;63:2397–410. 613

541 animals, including humans. At present mankind is faced with a [21] Martin-Creuzburg D, Wacker A, Basena T. Interactions between limiting nutri- 614
ents: consequences for somatic and population growth of Daphnia magna. 615
542 deficiency of these PUFA in diet. Since world rates of fisheries can- Limnol Oceanogr 2010;55:2597–607. 616
543 not be increased, additional sources of PUFA supply for humans, [22] Ahlgren G, Gustafsson IB, Boberg M. Fatty acid content and chemical compo- 617

544 such as aquaculture, biotechnology of microorganisms and genetic sition of freshwater microalgae. J Phycol 1992;28:37–50. 618
[23] Wenzel A, Bergstrom A-K, Jansson Ms Vrede T. Survival, growth and repro- 619
545 engineering of terrestrial oil-seed producing plants are developed. duction of Daphnia galeata feeding on single and mixed Pseudomonas and 620
546 However, natural fish production of aquatic ecosystems will remain Rhodomonas diets. Freshwater Biol 2012;57:835–46. 621

547 one of the main sources of EPA and DHA for humans. Thus, it [24] Chu FLE, Lund ED, Podbesek JA. Quantitative significance of n-3 essential fatty 622
acid contribution by heterotrophic protists in marine pelagic food webs. Mar 623
548 is necessary to estimate the potential role of different aquatic Ecol Prog Ser 2008;354:85–95. 624
549 ecosystems in diverse regions, inhabited by different fish species [25] Chen X, Wakeham SG, Fisher NS. Influence of iron on fatty acid and sterol com- 625
550 as sources and sinks of healthy, biochemically-valuable food for position of marine phytoplankton and copepod consumers. Limnol Oceanogr 626
2011;56:716–24. 627
551 human nutrition. Potential hazards which may reduce PUFA pro- [26] Chen M, Liu H, Chen B. Effects of dietary essential fatty acids on reproduction 628
552 duction in aquatic ecosystems, such as anthropogenically induced rates of a subtropical calanoid copepod, Acartia erythraea. Mar Ecol Prog Ser 629
553 eutrophication, pollution and climate warming must be studied, 2012;455:95–110. 630
[27] Muller-Navarra DC. Biochemical versus mineral limitation in Daphnia. Limnol 631
554 forecasted, and, where possible, prevented and mitigated.
Oceanogr 1995;40:1209–14. 632
[28] Wacker A, Becher P, Von Elert E. Food quality effects of unsaturated fatty 633
acids on larvae of the zebra mussel Dreissena polymorpha. Limnol Oceanogr 634
555 Acknowledgements 2002;47:1242–8. 635
[29] Arendt KE, Jonasdottir SH, Hansen PJ, Gartner S. Effects of dietary fatty acids 636

556 This work was supported by grants of Russian Foundation for on the reproductive success of the calanoid copepod Temora longicornis. Mar 637
Biol 2005;146:513–30. 638
557 Basic Research (RFBR) No. 11-04-00168 and No. 12-05-00298, and [30] Fleurence J, Gutbier G, Mabeaul S, Leray C. Fatty acids from 11 marine macroal- 639
558 also by the project B-15 of Siberian Federal University, carried out gae of the French Brittany coast. J Appl Phycol 1994;6:527–32. 640
559 according to Federal Tasks of Ministry of Education and Science of [31] Kalacheva GS, Sushchik NN, Gladyshev MI, Makhutova ON. Seasonal dynamics 641
of fatty acids in the lipids of water moss Fontinalis antipyretica from the Yenisei 642
560 Russian Federation. We are grateful to two anonymous reviewers River. Russ J Plant Physiol 2009;56:794–806. 643
561 for their helpful comments to improve the manuscript. [32] Olsson PA, Baath E, Jakobsen I, Soderstrom B. The use of phospholipid and 644
neutral lipid fatty acids to estimate biomass of arbuscular mycorrhizal fungi 645
in soil. Mycol Res 1995;99:623–9. 646
562 References [33] Debiane D, Calonne M, Fontaine J, Laruelle F, Grandmougin-Ferjani A, Lounes- 647
Hadj Sahraoui A. Lipid content disturbance in the arbuscular mycorrhizal, 648

563 [1] Lauritzen L, Hansen HS, Jorgensen MH, Michaelsen KF. The essentiality of long Glomus irregulare grown in monoxenic conditions under PAHs pollution. Fun- 649

564 chain n-3 fatty acids in relation to development and function of the brain and gal Biol 2011;115:782–92. 650

565 retina. Prog Lipid Res 2001;40:1–94. [34] Yu AQ, Zhu JC, Zhang B, Xing LJ, Li M. Effects of different carbon sources on 651

566 [2] Kris-Etherton PM, Harris WS, Appel LJ. Fish consumption, fish oil, omega-3 the growth, fatty acids production, and expression of three desaturase genes 652

567 fatty acids, and cardiovascular disease. Circulation 2002;106:2747–57. of Mortierella alpina ATCC 16266. Curr Microbiol 2011;62:1617–22. 653

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 ARTICLE IN PRESS
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PRO 6030 1–10

M.I. Gladyshev et al. / Prostaglandins & other Lipid Mediators xxx (2013) xxx–xxx 9

654 [35] Chang KJL, Dunstan GA, Abell GCJ, et al. Biodiscovery of new Australian thraus- [63] Pankhurst CE, Yu S, Hawke BG, Harch BD. Capacity of fatty acid profiles and 740
655 tochytrids for production of biodiesel and long-chain omega-3 oils. Appl substrate utilization patterns to describe differences in soil microbial com- 741
656 Microbiol Biotechnol 2012;93:2215–31. munities associated with increased salinity or alkalinity at three locations in 742
657 [36] Nichols DS, McMeekinl TA, Nichols PD. Manipulation of polyunsaturated, South Australia. Biol Fertil Soils 2001;33:204–17. 743
658 branchedchain and trans-fatty acid production in Shewanella putrefaciens [64] Williams MA, Myrold DD, Bottomley PJ. Carbon flow from 13 C-labeled straw 744
659 strain ACAM 342. Microbiology 1994;140:577–84. and root residues into the phospholipid fatty acids of a soil microbial com- 745
660 [37] Nichols DS, Nichols PD, Russell NJ, Davies NW, McMeekin TA. Polyunsaturated munity under field conditions. Soil Biol Biochem 2006;38:759–68. 746
661 fatty acids in the psychrophilic bacterium Shewanella gelidimarina ACAM [65] Ponnampalam EN, Sinclair AJ, Egan AR, Blakeley SJ, Leury BJ. Effect of diets 747
662 456T: molecular species analysis of major phospholipids and biosynthesis containing n-3 fatty acids on muscle long-chain n-3 fatty acid content in lambs 748
663 of eicosapentaenoic acid. BBA-Lipid Met 1997;1347:164–76. fed low- and medium-quality roughage diets. J Anim Sci 2001;79:698–706. 749
664 [38] Flores-Moya A, Fernandez JA. Seasonal variations of photosynthetic pigments, [66] Dannenberger D, Nuernberg K, Nuernberg G, Priepke A. Different dietary pro- 750
665 total C, N, and P content, and photosynthesis in Phyllariopsis purpurascens tein and pufa interventions alter the fatty acid concentrations, but not the 751
666 (Phaeophyta) from the Strait of Gibraltar. J Phycol 1995;31:867–74. meat quality, of porcine muscle. Nutrients 2012;4:1237–46. 752
667 [39] Henley WJ, Dunton KH. A seasonal comparison of carbon, nitrogen, and pig- [67] Kouba M, Benatmane F, Blochet JE, Mourot J. Effect of a linseed diet on lipid 753
668 ment content in Laminaria solidungula and L. saccharina (Phaeophyta) in the oxidation, fatty acid composition of muscle, perirenal fat, and raw and cooked 754
669 Alaskan Arctic. J Phycol 1995;31:325–31. rabbit meat. Meat Sci 2008;80:829–34. 755
670 [40] Gomez I, Wiencke C. Seasonal changes in C, N and major organic compounds [68] Mandell IB, Buchanan-Smith JG, Holub BJ, Campbell CP. Effects of fish meal 756
671 and their significance to morpho-functional processes in the endemic Antarc- in beef cattle diets on growth performance, carcass characteristics, and fatty 757
672 tic brown alga Ascoseira mirabilis. Polar Biol 1998;19:115–24. acid composition of longissimus muscle. J Anim Sci 1997;75:910–9. 758
673 [41] Gordillo FJL, Aguilera J, Jimenez C. The response of nutrient assimilation and [69] Gladyshev MI, Kharitonov AY, Popova ON, Sushchik NN, Makhutova ON, 759
674 biochemical composition of Arctic seaweeds to a nutrient input in summer. J Kalacheva GS. Quantitative estimation of dragonfly role in transfer of essential 760
675 Exp Bot 2006;57:2661–71. polyunsaturated fatty acids from aquatic to terrestrial ecosystems. Doklady 761
676 [42] Guschina IA, Harwood JL. Algal lipids and effect of the environment on their Biochem Biophys 2011;438:141–3. 762
677 biochemistry. In: Arts MT, Kainz M, Brett MT, editors. Lipids in aquatic ecosys- [70] Gladyshev MI, Sushchik NN, Yurchenko YA, Belevich OE, Kalacheva GS. Dif- 763
678 tems. New York: Springer; 2009. p. 1–24. ferences in the fatty acid compositions of blood-sucking mosquito larvae and 764
679 [43] Raven JA, Maberly SC. Plant productivity of inland waters. In: Papageorgiou imagoes and the water-to-land export of essential acids. Doklady Biol Sci 765
680 GC, Govindjee, editors. Chlorophyll a fluorescence. Advances in photosynthe- 2011;441:385–8. 766
681 sis and respiration, vol. 19. Dordrecht: Springer; 2004. p. 779–93. [71] Buckner JS, Hagen MM. Triacylglycerol and phospholipid fatty acids of the sil- 767
682 [44] Derieux S, Fillaux J, Saliot A. Lipid class and fatty acid distributions in par- verleaf whitefly: composition and biosynthesis. Arch Insect Biochem Physiol 768
683 ticulate and dissolved fractions in the north Adriatic Sea. Org Geochem 2003;53:66–79. 769
684 1998;29:1609–21. [72] Wang Y, Lin DS, Bolewicz L, Connor WE. The predominance of polyunsaturated 770
685 [45] Mannino A, Harvey HR. Lipid composition in particulate and dissolved organic fatty acids in the butterfly Morpho peleides before and after metamorphosis. 771
686 matter in the Delaware Estuary: sources and diagenetic patterns. Geochim J Lipid Res 2006;47:530–6. 772
687 Cosmochim Acta 1999;63:2219–35. [73] Pauly D, Christensen V. Primary production required to sustain global fish- 773
688 [46] Wichard T, Poulet SA, Boulesteix A-L, et al. Influence of diatoms on copepod eries. Nature 1995;374:255–7. 774
689 reproduction. II. Uncorrelated effects of diatom-derived ␣,␤,␥,␦-unsaturated [74] Gladyshev MI, Sushchik NN, Anishchenko OV, et al. Efficiency of transfer of 775
690 aldehydes and polyunsaturated fatty acids on Calanus helgolandicus in the essential polyunsaturated fatty acids versus organic carbon from producers 776
691 field. Progr Oceanogr 2008;77:30–44. to consumers in a eutrophic reservoir. Oecologia 2011;165:521–31. 777
692 [47] Koussoroplis A-M, Bec A, Perga M-E, Koutrakis E, Bourdier G, Desvilettes [75] Broadhurst CL, Wang Y, Crawford MA, Cunnane SC, Parkington JE, Schmidt 778
693 C. Fatty acid transfer in the food web of a coastal Mediterranean lagoon: WF. Brain-specific lipids from marine, lacustrine, or terrestrial food resources: 779
694 evidence for high arachidonic acid retention in fish. Estuar Coast Shelf Sci potential impact on early African Homo sapiens. Comp Biochem Phys B 780
695 2011;91:450–61. 2002;131:653–73. 781
696 [48] Gutseit K, Berglund O, Graneli W. Essential fatty acids and phosphorus in ses- [76] Gladyshev MI, Krylov AV, Sushchik NN, et al. Transfer of essential polyun- 782
697 ton from lakes with contrasting terrestrial dissolved organic carbon content. saturated fatty acids from an aquatic to terrestrial ecosystem through the 783
698 Freshwater Biol 2007;52:28–38. fish–bird trophic pair. Doklady Biol Sci 2010;431:121–3. 784
699 [49] Gladyshev MI, Semenchenko VP, Dubovskaya OP, et al. Effect of tempera- [77] Kris-Etherton PM, Grieger JA, Etherton TD. Dietary reference intakes for DHA 785
700 ture on contents of essential highly unsaturated fatty acids in freshwater and EPA. Prostaglandins Leukot Essent Fatty Acids 2009;81:99–104. 786
701 zooplankton. Limnologica 2011;41:339–47. [78] Reis LC, Hibbeln JR. Cultural symbolism of fish and the psychotropic prop- 787
702 [50] Gladyshev MI, Arts MT, Sushchik NN. Preliminary estimates of the export of erties of omega-3 fatty acids. Prostaglandins Leukot Essent Fatty Acids 788
703 omega-3 highly unsaturated fatty acids (EPA + DHA) from aquatic to terres- 2006;75:227–36. 789
704 trial ecosystems. In: Arts MT, Kainz M, Brett MT, editors. Lipids in aquatic [79] Harris WS, Mozaffarian D, Lefevre M, et al. Towards establishing dietary 790
705 ecosystems. New York: Springer; 2009. p. 179–209. reference intakes for eicosapentaenoic and docosahexaenoic acids. J Nutr 791
706 [51] Kimura H, Fukuba T, Naganuma T. Biomass of thraustochytrid protoctists in 2009;139, 804S–19S. 792
707 coastal water. Mar Ecol Prog Ser 1999;189:27–33. [80] Pauly D, Christensen V, Guenette S, et al. Towards sustainability in world 793
708 [52] Raghukumar S. Ecology of the marine protists, the Labyrinthulomycetes fisheries. Nature 2002;418:689–95. 794
709 (Thraustochytrids and Labyrinthulids). Europ J Protistol 2002;38:127–45. [81] De Silva SS. Aquaculture: a newly emergent food production sector—and per- 795
710 [53] Raghukumar S, Ramaiah N, Raghukumar C. Dynamics of thraustochytrid spectives of its impacts on biodiversity and conservation. Biodivers Conserv 796
711 protists in the water column of the Arabian Sea. Aquat Microb Ecol 2012;21:3187–220. 797
712 2001;24:175–86. [82] Sijtsma L, de Swaaf ME. Biotechnological production and applications of 798
713 [54] Jain R, Raghukumar S, Sambaiah K, Kumon Y, Nakahara T. Docosahexaenoic the ␻-3 polyunsaturated fatty acid docosahexaenoic acid. Appl Microbiol 799
714 acid accumulation in thraustochytrids: search for the rationale. Mar Biol Biotechnol 2004;64:146–53. 800
715 2007;151:1657–64. [83] Mendes A, Reis A, Vasconcelos R, Guerra P, Lopes da Silva T. Cryptheco- 801
716 [55] Fan KW, Jiang Y, Faan YW, Chen F. Lipid characterization of mangrove dinium cohnii with emphasis on DHA production: a review. J Appl Phycol 802
717 thraustochytrid – Schizochytrium mangrovei. J Agric Food Chem 2007;55: 2009;21:199–214. 803
718 2906–10. [84] Khozin-Goldberg I, Iskandarov U, Cohen Z. LC-PUFA from photosynthetic 804
719 [56] Kimura H, Sato M, Sugiyama C, Naganuma T. Coupling of thraustochytrids microalgae: occurrence, biosynthesis, and prospects in biotechnology. Appl 805
720 and POM, and of bacterio- and phytoplankton in a semi-enclosed coastal area: Microbiol Biotechnol 2011;91:905–15. 806
721 implication for different substrate preference by the planktonic decomposers. [85] Raghukumar S. Thraustochytrid marine protists: production of PUFAs and 807
722 Aquat Microb Ecol 2001;25:293–300. other emerging technologies. Mar Biotechnol 2008;10:631–40. 808
723 [57] Cao Y, Cao Y, Zhao M. Biotechnological production of eicosapentaenoic [86] Rubio-Rodriguez N, Beltran S, Jaime I, de Diego SM, Sanz M, Carballido JR. 809
724 acid: from a metabolic engineering point of view. Process Biochem Production of omega-3 polyunsaturated fatty acid concentrates: a review. 810
725 2012;47:1320–6. Innov Food Sci Emerg 2010;11:1–12. 811
726 [58] Kastovska K, Stibal M, Sabacka M, Cerna B, Santrucova H, Elster J. Microbial [87] Damude HG, Kinney AJ. Engineering oilseed plants for a sustainable, 812
727 community structure and ecology of subglacial sediments in two polyther- land-based source of long chain polyunsaturated fatty acids. Lipids 813
728 mal Svalbard glaciers characterized by epifluorescence microscopy and PLFA. 2007;42:179–85. 814
729 Polar Biol 2007;30:277–87. [88] Robert SS. Production of eicosapentaenoic and docosahexaenoic acid- 815
730 [59] Rillig MC. Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecol containing oils in transgenic land plants for human and aquaculture nutrition. 816
731 Lett 2004;7:740–54. Mar Biotechnol 2006;8:103–9. 817
732 [60] Sampedro L, Jeannotte R, Whalen JK. Trophic transfer of fatty acids from [89] Sushchik NN, Kalacheva GS, Zhila NO, Gladyshev MI, Volova TG. A temperature 818
733 gut microbiota to the earthworm Lumbricus terrestris L. Soil Biol Biochem dependence of the intra- and extracellular fatty-acid composition of green 819
734 2006;38:2188–98. algae and cyanobacterium. Russ J Plant Physiol 2003;50:374–80. 820
735 [61] Tanaka T, Ikita K, Ashida T, Motoyama Y, Yamaguchi Y, Satouchi K. Effects of [90] Petkov G, Garcia G. Which are fatty acids of the green alga Chlorella. Biochem 821
736 growth temperature on the fatty acid composition of the free-living nematode Syst Ecol 2007;35:281–5. 822
737 Caenorhabditis elegans. Lipids 1996;31:1173–8. [91] Iliev I, Petkov G, Lukavsky J, Furnadzhieva S, Andreeva R. Do cyanobacte- 823
738 [62] Vishnevetsky S. Phospholipid fatty acid (PLFA) composition and its dynamics rial lipids contain fatty acids longer than 18 carbon atoms. Z Naturforsch C 824
739 in a desert soil system. Arid Soil Res Rehabilit 2000;14:59–68. 2011;66:267–76. 825

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 ARTICLE IN PRESS
G Model
PRO 6030 1–10

10 M.I. Gladyshev et al. / Prostaglandins & other Lipid Mediators xxx (2013) xxx–xxx

826 [92] Gulati RD, Dionisio Pires LM, Van Donk E. Lake restoration studies: failures, Shira, a brackish water body in Southern Siberia. J Siberian Federal Univ Biol 882
827 bottlenecks and prospects of new ecotechnological measures. Limnologica 2011;4:86–103. 883
828 2008;38:233–47. [111] Sushchik NN, Gladyshev MI, Kalachova GS, Makhutova ON, Ageev AV. Com- 884
829 [93] Gladyshev MI, Anishchenko OV, Sushchnik NN, Kalacheva GS, Gribovskaya parison of seasonal dynamics of the essential PUFA contents in benthic 885
830 IV, Ageev AV. Influence of anthropogenic pollution on content of essential invertebrates and grayling Thymallus arcticus in the Yenisei river. Comp 886
831 polyunsaturated fatty acids in links of food chain of river ecosystem. Contemp Biochem Phys B 2006;145:278–87. 887
832 Probl Ecol 2012;5:376–85. [112] Lee RF, Hagen W, Kattner G. Lipid storage in marine zooplankton. Mar Ecol 888
833 [94] Brett MT, Muller-Navarra DC, Persson J. Crustacean zooplankton fatty acid Prog Ser 2006;307:273–306. 889
834 composition. In: Arts MT, Kainz M, Brett MT, editors. Lipids in aquatic ecosys- [113] Philibert A, Vanier C, Abdelouahab N, Chan HM, Donna Mergler D. Fish 890
835 tems. New York: Springer; 2009. p. 115–46. intake and serum fatty acid profiles from freshwater fish. Am J Clin Nutr 891
836 [95] Tocher DR. Metabolism and functions of lipids and fatty acids in teleost fish. 2006;84:1299–307. 892
837 Rev Fish Sci 2003;11:107–84. [114] Makhutova ON, Sushchik NN, Gladyshev MI, Ageev AV, Pryanichnikova EG, 893
838 [96] Jeppesen E, Meerhoff M, Holmgren K, et al. Impacts of climate warming on Kalachova GS. Is the fatty acid composition of freshwater zoobenthic inver- 894
839 lake fish community structure and potential effects on ecosystem function. tebrates controlled by phylogenetic or trophic factors? Lipids 2011;46: 895
840 Hydrobiologia 2010;646:73–90. 709–21. 896
841 [97] Huynh MD, Kitts DD. Evaluating nutritional quality of pacific fish species from [115] Lau DCP, Vrede T, Pickova J, Goedkoop W. Fatty acid composition of consumers 897
842 fatty acid signatures. Food Chem 2009;114:912–8. in boreal lakes – variation across species, space and time. Freshwater Biol 898
843 [98] Chuang LT, Bulbul U, Wen PC, Glew RH, Ayaz FA. Fatty acid composition of 12 2012;57:24–38. 899
844 fish species from the Black Sea. J Food Sci 2012;77:512–8. [116] Zenebe T, Ahlgren G, Boberg M. Fatty acid content of some freshwater fish of 900
845 [99] Kitson AP, Patterson AC, Izadi H, Stark KD. Pan-frying salmon in an eicos- commercial importance from tropical lakes in the Ethiopian Rift Valley. J Fish 901
846 apentaenoic acid (EPA) and docosahexaenoic acid (DHA) enriched margarine Biol 1998;53:987–1005. 902
847 prevents EPA and DHA loss. Food Chem 2009;114:927–32. [117] Rocha DN, Simoes LN, Paiva G, Gomes LC. Sensory, morphometric and prox- 903
848 [100] Gladyshev MI, Sushchik NN, Gubanenko GA, Demirchieva SM, Kalachova GS. imate analyses of Nile tilapia reared in ponds and net-cages. R Bras Zootec 904
849 Effect of way of cooking on content of essential polyunsaturated fatty acids 2012;41:1795–9. 905
850 in muscle tissue of humpback salmon (Oncorhynchus gorbuscha). Food Chem [118] Gladyshev MI, Gribovskaya IV, Moskvicheva AV, Muchkina EY, Chuprov SM, 906
851 2006;96:446–51. Ivanova EA. Content of metals in compartments of ecosystem of a Siberian 907
852 [101] Heissenberger M, Watzke J, Kainz MJ. Effect of nutrition on fatty acid pro- pond. Arch Environ Con Tox 2001;41:157–62. 908
853 files of riverine, lacustrine, and aquaculture-raised salmonids of pre-alpine [119] Foran JA, Good DH, Carpenter DO, Hamilton MC, Knuth BA, Schwager SJ. 909
854 habitats. Hydrobiologia 2010;650:243–54. Quantitative analysis of the benefits and risks of consuming farmed and wild 910
855 [102] Wagner T, Jones ML, Ebener MP, et al. Spatial and temporal dynamics of salmon. J Nutr 2005;135:2639–43. 911
856 lake whitefish (Coregonus clupeaformis) health indicators: linking individual- [120] Zotina T, Trofimova E, Bolsunovsky A. Artificial radionuclides in fish fauna of 912
857 based indicators to a management-relevant endpoint. J Great Lakes Res the Yenisei River in the vicinity of the mining-and-chemical combine (Siberia, 913
858 2010;36:121–34. Russia). Radioprotection 2011;46:75–8. 914
859 [103] Ahlgren G, Blomqvist P, Boberg M, Gustafsson I-B. Fatty acid content of the [121] Trofimova EA, Zotina TA, Bolsunovskii AY. Estimation of transfer of techno- 915
860 dorsal muscle – an indicator of fat quality in freshwater fish. J Fish Biol genic radionuclides in food chains of the Yenisei River. Contemp Probl Ecol 916
861 1994;45:131–57. 2012;5:365–70. 917
862 [104] Sushchik NN, Gladyshev MI, Kalachova GS. Seasonal dynamics of fatty acid [122] Gladyshev MI, Sushchik NN, Anishchenko OV, Makhutova ON, Kalachova GS, 918
863 content of a common food fish from the Yenisei River, Siberian grayling, Gribovskaya IV. Benefit-risk ratio of food fish intake as the source of essential 919
864 Thymallus arcticus. Food Chem 2007;104:1353–8. fatty acids vs. heavy metals: a case study of Siberian grayling from the Yenisei 920
865 [105] Gladyshev MI, Lepskaya EV, Sushchik NN, et al. Comparison of polyunsat- River. Food Chem 2009;115:545–50. 921
866 urated fatty acids content in filets of anadromous and landlocked sockeye [123] Candela M, Astiasaran I, Bello J. Deep-fat frying modifies high-fat fish lipid 922
867 salmon Oncorhynchus nerka. J Food Sci 2012;77:1306–10. fraction. J Agr Food Chem 1998;46:2793–6. 923
868 [106] Maulvault AL, Anacleto P, Machado R, et al. Effect of sex, maturation stage and [124] Tarley CRT, Visentainer JV, Matsushita M, de Souza NE. Proximate com- 924
869 cooking methods on the nutritional quality and safety of black scabbard fish position, cholesterol and fatty acids profile of canned sardines (Sardinella 925
870 (Aphanopus carbo Lowe, 1839). J Sci Food Agric 2012;92:1545–53. brasiliensis) in soybean oil and tomato sauce. Food Chem 2004;88:1–6. 926
871 [107] Ozyurt G, Pola A, Ozkutuk S. Seasonal changes in the fatty acids of gilthead [125] Sampaio GR, Bastos DHM, Soares RAM, Queiroz YS, Torres EAFS. Fatty 927
872 sea bream (Sparus aurata) and white sea bream (Diplodus sargus) captured in acids and cholesterol oxidation in salted and dried shrimp. Food Chem 928
873 Iskenderun Bay, eastern Mediterranean coast of Turkey. Eur Food Res Technol 2006;95:344–51. 929
874 2005;220:120–4. [126] Gladyshev MI, Sushchik NN, Makhutova ON, Kalachova GS. Content of essen- 930
875 [108] Kwetegyeka J, Mpango G, Grahl-Nielsen O. Variation in fatty acid composition tial polyunsaturated fatty acids in three canned fish species. Int J Food Sci 931
876 in muscle and heart tissues among species and populations of tropical fish in Nutr 2009;60:224–30. 932
877 lakes Victoria and Kyoga. Lipids 2008;43:1017–29. [127] Sioen I, Haak L, Raes K, et al. Effects of pan-frying in margarine and olive oil on 933
878 [109] Gladyshev MI, Sushchik NN, Gubanenko GA, Demirchieva SM, Kalachova GS. the fatty acid composition of cod and salmon. Food Chem 2006;98:609–17. 934
879 Effect of boiling and frying on the content of essential polyunsaturated fatty [128] Simon SJGB, Sancho RAS, Lima FA, et al. Interaction between soybean oil and 935
880 acids in muscle tissue of four fish species. Food Chem 2007;101:1694–700. the lipid fraction of fried pitu prawn. LWT-Food Sci Technol 2012;48:120–6. 936
881 [110] Rogozin DY, Pulyayevskaya MV, Zuev IV, Makhutova ON, Degermendzhi AG. [129] Haak L, Sioen I, Raes K, Van Camp J, De Smet S. Effect of pan-frying in different 937
Growth, diet and fatty acid composition of Gibel carp Carassius gibelio in Lake culinary fats on the fatty acid profile of pork. Food Chem 2007;102:857–64. 938

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