Lipids (2008) 43:461–466 DOI 10.1007/s11745-008-3166-5
COMMUNICATION
From Aquatic to Terrestrial Food Webs: Decrease of the Docosahexaenoic Acid/Linoleic Acid Ratio Apostolos-Manuel Koussoroplis Æ Charles Lemarchand Æ Alexandre Bec Æ Christian Desvilettes Æ Christian Amblard Æ Christine Fournier Æ Philippe Berny Æ Gilles Bourdier
Received: 26 November 2007 / Accepted: 22 February 2008 / Published online: 12 March 2008 Ó AOCS 2008
Abstract Fatty acid composition of the adipose tissue of six carnivorous mammalian species (European otter Lutra lutra, American mink Mustela vison, European Mink Mustela lutreola, European polecat Mustela putorius, stone marten Martes foina and European wild cat Felis silvestris) was studied. These species forage to differing degrees in aquatic and terrestrial food webs. Fatty acid analysis revealed significant differences in polyunsaturated fatty acid composition between species. More specifically, our results underline a gradual significant decrease in the docosahexaenoic acid (DHA)/linoleic acid (LNA) ratio of carnivore species as their dependence on aquatic food webs decreases. In conclusion, the use of the DHA/LNA ratio in long-term studies is proposed as a potential proxy of changes in foraging behaviour of semiaquatic mammals. Keywords Biomarkers Carnivorous mammals Conservation Diet Docosahexaenoic acid Fatty acids Food webs Linoleic acid Peritoneal fat
A.-M. Koussoroplis (&) C. Lemarchand A. Bec C. Desvilettes C. Amblard G. Bourdier Laboratoire LMGE, UMR CNRS 6023, Equipe Re´seaux Trophiques Aquatiques, Universite´ Blaise Pascal, 24, Avenue des Landais, 63177 Aubie`re, France e-mail:
[email protected] C. Fournier GREGE, Route de Pre´chac, 33730 Villandraut, France P. Berny Laboratoire de Biologie et Toxicologie, ENVL, BP83, 69280 Marcy l’Etoile, France
Abbreviations ARA Arachidonic acid ALA a-Linolenic acid DHA Docosahexaenoic acid EPA Eicosapentaenoic acid LNA Linoleic acid MUFA Monounsaturated fatty acid PUFA Polyunsaturated fatty acid SAFA Saturated fatty acid TFAW Total fatty acid weight
Introduction Recent legal protection and conservation programs allowed many endangered species to re-colonise their habitats. Nevertheless, these species have to cope now with disturbed biotopes and prey populations. The re-colonising success of these species in their disturbed niches suggests a change in their foraging strategies [1, 2]. However, these diet modifications are very difficult to evaluate in a low density context [3]. Indeed, direct observation of faeces analysis give only a snapshot of the animals’ diet. On the other hand, fatty acid storage tissue composition has been successfully used in many cases as an accurate and time-integrating proxy of carnivorous mammals’ diets [4–7]. The latter is based on the fact that some dietary fatty acids are stored in the adipose tissues without important modifications and thus can be used as biomarkers [4]. Lipids from aquatic and terrestrial primary producers exhibit differences in fatty acid signatures [8]. Phytoplanktonic microalgae can produce n-3 polyunsaturated fatty acids (PUFAs) in large quantities [8–11]. In contrast, few terrestrial plants (e.g. Berries, Olives) contain significant amounts of a-linolenic acid (18:3n-3, ALA), whereas many
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more synthesize and store large amounts of linoleic acid (18:2n-6, LA) [12]. Highly unsaturated PUFAs (e.g. 20:4n6; ARA, 20:5n-3; EPA, 22:6n-3; DHA) are involved in a wide range of physiological processes. As most animals lack the specific fatty acid desaturases required to insert double bonds in the n-3 and the n-6 position, these compounds have to be obtained by the animals from their diet [13, 14]. This results in a high conservation of these molecules along food webs, from primary producers to final consumers [15, 16]. Consequently, each type of food web shows a ‘‘typical’’ fatty acid profile [17, 18]. In aquatic food webs n-3 PUFAs dominate over n-6 PUFAs by a factor of 5–20 [17, 19]. The opposite is true for terrestrial food webs where n-6 PUFAs are more abundant than n-3 PUFAs [20]. Thus, we expect that gradual transitions from one food web to another are followed by a gradual evolution of fatty acid proportions The major aim of this study is to investigate the evolution of PUFA patterns along a gradual transition from aquatic to terrestrial food webs. In this context, fatty acid composition of the peritoneal fat of six carnivore species (Mammalia, Carnivora) was analysed. The analysed species (European otter Lutra lutra, Linnaeus 1758 American mink Mustela vison, Schreber 1777, European mink Mustela lutreola, Linnaeus 1761, European polecat Mustela putorius, Linnaeus 1758, Stone marten Martes foina, Erxleben 1777 and European wild cat Felis sylvestris, Schreber 1777) were chosen in order to illustrate a continuous decreasing gradient of aquatic food web exploitation (Fig. 1).
Materials and Methods
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chosen in the Mustelidae family: (American mink, n = 13; European otter, n = 17; European mink, n = 17; European polecat, n = 13; stone marten, n = 13) and one species was chosen in the Felidae family (European wild cat, n = 14). For ethical, legal and technical reasons, only freshly conserved (maximum 24 h) wild animals killed by road traffic were collected, using existent French networks in animal studies. Peritoneal adipose tissues were sampled and deepfrozen (-80 °C) before the lipid analysis. Lipid and Statistical Analysis Total lipids were extracted from tissue samples with a chloroform/methanol (2:1, v/v) mixture [21]. Fatty acid methyl esters were obtained by hydrolysis in methanolic NaOH and esterification in methanolic H2SO4 [10]. Fatty acid analyses were carried out on a Chrompack CP 9001 gas chromatograph equipped with a SupelcoÒ OmegacoaxTM column and a FID detector (260 °C) (split injection; injector temperature: 260 °C; carrier gas: helium; oven rise from 140 to 245 °C at 3 °C min-1). Individual fatty acid methyl esters are identified by comparing retention times with those obtained from SupelcoÒ standards and laboratory standards. Fatty acid methyl esters were quantified using 13:0 as an internal standard that is added before the derivation of fatty acids. Statistical differences in DHA, LNA and DHA/LNA compositions among sampled species were analysed with the Kruskal–Wallis test and when significant, two-by-two species comparisons were made with the Mann–Whitney U test. Correlation was calculated with Spearman’s correlation coefficient (rs). P values less than 0.05 where considered significant.
Carnivore Sampling Results and Discussion Six species of two families of carnivores were chosen in order to illustrate a continuous decreasing gradient of aquatic food web exploitation (Fig. 1), and sampled in France between 2002 and 2006. Species were mainly
Fig. 1 Schematic representation of food source origin of the studied carnivorous mammals. White: fish; clear grey: crayfish; dark grey: amphibians; black: terrestrial food (birds, mammals, fruits, terrestrial invertebrates); Data synthesised from previous studies [35–39]
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SAFA and MUFA Patterns A total of 87 individuals were analysed for fatty acid composition (Table 1). Saturated fatty acids (SAFA) varied from 29.3 (European otter) to 55.3% (stone marten) of the total fatty acids weight (TFAW). As already observed [4, 22] for other mammals, SAFA are dominated by 16:0 (17.2% of the TFAW for otter, 31.4% for stone marten) and to a lesser extent by 18:0 (4.9% of the TFAW for otter to 22.8% of the TFAW for stone marten). The monounsaturated fatty acids (MUFA) ranged from 21.4 (stone marten) to 45.0% (European mink) of TFAW. As observed for other carnivorous mammals [4, 22, 23] 18:1n-9 was the dominant fatty acid in MUFA, varying from 20.0 (stone marten) to 40.6% (European mink) of TFAW. Substantial or high levels of 16:1n-7 were also observed, ranging from 1.4 (stone marten) to 8.3% (European otter).
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Table 1 Fatty acid composition of peritoneal adipose tissue of the six carnivorous mammal species studied
14:0
Lutra lutra (n = 17)
Mustela vison (n = 13)
Mustela lutreola (n = 17)
Mustela putorius (n = 13)
Martes foina (n = 13)
Felis silvestris (n = 14)
4.0 ± 1.8
3.8 ± 1.8
2.5 ± 0.8
2.9 ± 0.8
1.1 ± 1.2
1.5 ± 1.2
15:0
1.0 ± 0.5
3.5 ± 3.0
Tr
0.6 ± 0.3
Tr
2.1 ± 1.9
16:0
17.2 ± 3.6
18.4 ± 8.6
20.5 ± 3.5
18.8 ± 3.4
31.4 ± 10.5
19.3 ± 4.7
17:0
0.8 ± 0.3
0.6 ± 0.3
0.5 ± 0.3
0.8 ± 0.5
Tr
1.1 ± 1.4
18:0
4.9 ± 1.9
8.5 ± 1.2
8.9 ± 2.9
16.3 ± 16.1
22.8 ± 7.3
10.6 ± 4.4
20:0
Tr
Tr
Tr
Tr
–
Tr
Br. SAFA SAFA
1.4 ± 1.1 29.3 ± 5.3
Tr 34.8 ± 4.9
Tr 32.4 ± 5.0
Tr 39.4 ± 14.5
– 55.3 ± 9.3
Tr 34.6 ± 8.7 2.0 ± 0.6
16:1n-7
8.3 ± 3.2
3.7 ± 1.5
3.4 ± 1.8
2.1 ± 1.1
1.4 ± 1.1
18:1n-7
1.6 ± 2.2
–
Tr
Tr
Tr
Tr
18:1n-9
28.4 ± 2.7
37.6 ± 7.2
40.6 ± 10.1
27.0 ± 9.7
20.0 ± 7.1
38.5 ± 14.0
20:1n-11 + 1n-9
1.7 ± 1.0
1.1 ± 0.7
1.0 ± 0.7
Tr
Tr
0.6 ± 0.5
MUFA
40.0 ± 4.9
42.4 ± 7.4
45.0 ± 9.2
29.1 ± 10.9
21.4 ± 7.3
41.1 ± 14.3
16:2n-4
Tr
–
–
–
–
–
16:3n-4
0.9 ± 0.6
Tr
Tr
Tr
–
Tr
18:2n-6*
10.6 ± 2.8
15.2 ± 5.5
14.8 ± 4.4
18.2 ± 4.4
11.1 ± 3.3
15.9 ± 5.1
18:3n-6
Tr
Tr
Tr
Tr
Tr
Tr
18:3n-3
4.0 ± 2.2
1.8 ± 1.2
1.7 ± 1.1
7.3 ± 7.9
Tr
2.6 ± 2.8
18:4n-3
Tr
–
–
–
–
– Tr
20:2n-6
0.8 ± 0.4
Tr
Tr
0.6 ± 0.5
Tr
20:3n-6
0.6 ± 0.4
Tr
Tr
Tr
1.0 ± 0.9
Tr
20:4n-6
2.2 ± 1.0
1.0 ± 0.6
1.1 ± 0.6
1.2 ± 1.0
5.5 ± 4.3
2.3 ± 3.8
20:3n-3
Tr
Tr
Tr
Tr
–
Tr
20:4n-3
Tr
Tr
–
–
–
–
20:5n-3
1.2 ± 0.9
Tr
Tr
Tr
Tr
Tr
22:4n-6
0.9 ± 0.5
Tr
0.6 ± 0.4
0.5 ± 0.3
1.3 ± 1.3
Tr
22:5n-6
Tr
Tr
0.6 ± 0.4
Tr
Tr
Tr
22:5n-3
2.7 ± 0.7
0.9 ± 0.5
0.8 ± 0.6
1.3 ± 0.8
2.5 ± 1.9
1.6 ± 1.5
22:6n-3*
4.4 ± 1.2
1.2 ± 0.8
1.1 ± 0.7
0.6 ± 0.3
Tr
Tr 22.4 ± 9.2
PUFA
28.3 ± 4.6
20.1 ± 6.8
20.7 ± 6.4
29.7 ± 9.3
21.4 ± 7.3
NI
0.9 ± 0.8
Tr
Tr
Tr
Tr
Tr
Sum n-3
12.3 ± 2.4
3.9 ± 2.2
3.6 ± 2.3
9.2 ± 8.4
2.5 ± 2.1
4.2 ± 4.3
Sum n-6
15.1 ± 3.9
16.2 ± 6.1
17.1 ± 5.2
20.3 ± 5.2
18.9 ± 6.3
18.2 ± 6.6
22:6/18:2*
0.46 ± 0.22
0.09 ± 0.07
0.08 ± 0.06
0.04 ± 0.02
0.01 ± 0.02
0.02 ± 0.04
Values are the mean percentages of total fatty acid weight (TFAW) ± standard deviations Tr trace amounts (\0.5% TFAW), Br. SAFA sum of branched saturated fatty acids, MUFA sum of mono unsaturated fatty acids, PUFA sum of poly unsaturated fatty acids, – not detected, NI not identified * Significant difference amongst six studied species Kruskall–Wallis P \ 0.001 (only for 18:2n-6, 22:6n-3 and 22:6/18:2)
Variations in PUFA Patterns The polyunsaturated fatty acids (PUFA) make up 20.1% (American mink) to 29.7% (European polecat) of TFAW, and are dominated by the n-6 FAs (52.4–89.1% of the total weight of PUFA, data not shown). For all sampled species, 18:2n-6 (linoleic acid, LA) counts for more than half of the weight of n-6 PUFAs (data not shown). High concentrations of LNA (from 10.6 to 18.2% of TFAW for otter and
polecat, respectively) were also observed in terrestrial mammalian carnivores in previous studies [4, 24] and certainly reflect the abundance of this FA in terrestrial food webs [12, 18]. In contrast, n-3 FAs show stronger variations ranging from 10.9% (stone marten) to 42.5% (European otter) of total PUFA weight (data not shown) and are dominated by 18:3n-3 (a-linolenic acid, ALA) as well as by 22:6n-3 (docosahexaenoic acid, DHA) and to a lesser extent by
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Lipids (2008) 43:461–466
consumption. Indeed, the results suggest that important ALA amounts of aquatic origin are associated with high DHA amounts, as observed for the European otter and both mink species (Fig. 2). Moreover, European polecats rarely consume fish (Fig. 1) and ALA could come from berries consumption, since berries are known to contain significant amounts of ALA [12]. Furthermore, the European polecat is known to complete its diet with fruits and berries (Fig. 1). In contrast with DHA, the LNA concentration tends to be increased in carnivorous mammals with more ‘‘terrestrial’’ diets (Fig. 2). The DHA/LNA Ratio Fig. 2 Mean values of four major PUFAs in the peritoneal adipose tissue of the sampled carnivorous mammals, according to their degree of aquatic food web exploitation. For simplification reasons only the DHA and LNA statistical differences are presented. Data labelled with the same letter are not significantly different (Mann–Whitney, P \ 0.05)
22:5n-3 (Table 1). Species with aquatic prey-based diet (Fig. 1) show up to tenfold higher concentrations of DHA than species that predate exclusively on terrestrial prey (Fig. 2). A dietary-influence of DHA and EPA concentrations linked to fish consumption has already been documented for American minks kits fed on a fish-oil supplemented diet [4]. Indeed, DHA is abundant in both marine and freshwater fishes [14, 19]. Although freshwater fishes can also be a source of ALA [8, 25, 26] the high concentration of this FA observed for the European polecat (7.3% of TFAW) is probably not completely due to fish Fig. 3 Mean values of DHA/ LNA ratio in adipose tissue of carnivorous mammals belonging to different food webs. Dagger: data estimated from Samuel and Worthy [33]; double dagger data estimated from Ka¨kela¨ and Hyva¨rinen [23]; asterisks data estimated from Grahl-Nielsen et al. [22]. No symbol: data from present study. Above: DHA/LNA ratio in peritoneal adipose tissue of carnivorous mammals from this study. Data labelled with the same letter are not significantly different (Mann–Whitney, P \ 0.05)
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The decrease in DHA as well as the increasing tendency of LNA in carnivorous mammals from aquatic to terrestrial food webs seems to be confirmed when comparing our results to those from other studies (Fig. 3). Indeed, animals foraging strictly in aquatic food webs, such as dolphins or marine seals, are characterized by the highest DHA/LNA ratios whereas freshwater seals exhibit lower DHA/LNA ratios when compared to marine mammals. A previous study successfully used the n-3/n-6 fatty acid ratio to distinguish marine from freshwater populations of genetically related seals [23]. The great abundance of n-6 PUFAs in freshwater food webs has been suggested to be due to a greater terrestrial input of organic matter [18]. Indeed, river food webs are often based on the use of terrestrial plant detrital material by macroinvertebrates [27]. Moreover, in lakes, a recent study has suggested that 22–55% of assimilated carbon by the major freshwater ‘‘herbivore’’ Daphnia sp. is derived from terrestrial organic matter [28]
Lipids (2008) 43:461–466
which could be rich in LNA [29]. Thus, inputs of terrestrial organic matter could partially explain the abundance of n-6 PUFAs and more particularly LNA in freshwater food webs. However, terrestrial influence may also occur under the form of phosphorus loading. It has recently been shown that sestonic concentrations of n-3 highly unsaturated fatty acids (such as DHA or EPA) decreased along a trophic state gradient from oligotrophic to eutrophic lakes [30]. For evident reasons the authors established the decrease of DHA with increasing total phosphorus by sampling different lakes. It is tempting to speculate that the decrease of DHA could occur in a given lake over a long-term temporal scale corresponding to its natural eutrophication. This could imply that the DHA/LNA ratios that are observed in a given aquatic food web gradually evolve towards more terrestrial values. However, Mu¨ller-Navarra et al. [30] did not mention any increase of LNA with increasing total phosphorus. Nevertheless, phytoplankton composition in eutrophic lakes is often dominated by Cyanobacteria or Chlorophyceae, which do not produce DHA but can contain relatively high amounts of LNA [9, 31].
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among and within species. Moreover, more attention should be paid on adipose tissue turnover rates in order to establish more precisely the links between DHA/LNA ratio and dietary shifts. Once these parameters are known, it should be possible to determine whether the striking difference in the DHA/LNA ratios between otters and freshwater seals (Fig. 3) is relevant. If so, our results could suggest that the re-colonising otters sampled for this study are more strongly connected to terrestrial food webs than expected. This phenomenon has already been observed for American minks sharing the same biotope with otters. These two species are niche competitors, and their competition in a disturbed biotope can result in a switch of the mink’s diet from aquatic to terrestrial prey [1, 34]. In conclusion, we suggest that the DHA/LNA ratio is a useful tool for the assessment of the dietary plasticity of carnivorous mammals. The use of the DHA/LNA ratio in long-term studies could allow to evaluate in which manner changes in foraging behaviour are linked to population dynamics of semi-aquatic species in different geographical areas.
DHA/LNA Ratio Gradient from Aquatic to Terrestrial Food Webs References Because of the terrestrial influence and specific processes occurring in freshwater food webs, the DHA/LNA ratio can distinguish marine from freshwater mammals. For example, dolphins and seals foraging in marine food webs exhibit high DHA/LNA ratios ranging from 11 (Bottlenose dolphin Tursiops truncatus) to 11.82 (Ringed seal Phoca hispida), whereas freshwater seals exhibit ratios ranging from 2.5 to 5.29 (Fig. 3). Continental carnivorous mammals foraging partially or totally in terrestrial food webs exhibit much lower DHA/LNA ratios, ranging from 0.46 (European otter) to 0.01 (stone marten). More interestingly, the gradual decrease of the ratio is correlated with decreasing aquatic food web exploitation (rs = 0.957, P \ 0.05) (Fig. 3). The decrease in the DHA/LNA ratio from aquatic to terrestrial food webs led us to consider DHA/LNA ratio of carnivorous mammals as a proxy evaluating their connection strength to these two types of food webs. Nevertheless, the mean values of the DHA/LNA ratio of the animals sampled in this study exhibit an important individual variability (Fig. 3). As these animals were collected in different geographic areas and at different seasons, this variability could reflect geographical and temporal differences in foraging behaviour [32]. Furthermore, other parameters such as age, sex or physiological state should also be taken into account when considering this variability [22, 33]. Thus, further studies are required to better understand the dietary FA accumulation patterns and their variations
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