The trophic blockage hypothesis is not supported by the diets of fishes on Seine Seamount


Stefanie Hirch, Institute of Hydrobiology and Fishery Science, University of Hamburg, Große Elbstraße 133, D-22767 Hamburg, Germany.


Several hypotheses exist about the trophic mechanisms that support fish stocks at seamounts. This study investigated the diets of benthopelagic fish species on the summit plateau of Seine Seamount (NE Atlantic), testing the sound-scattering layer interception hypothesis. A combined approach of gut content, stable isotopes and fatty-acid biomarker analyses was employed. Fish species included zooplanktivores, benthivores, piscivores and species with mixed crustacean/cephalopod/fish diets. Trophic coupling between pelagic food sources and benthopelagic fish consumers was apparent based on three main lines of evidence: (i) dominance of pelagic prey in the guts of zooplanktivores, (ii) stable isotope enrichment of consumers indicative of a pelagic prey source, and (iii) high proportions of fatty acids that are typical of phytoplankton and zooplankton in the storage lipids of fishes and their similarity with fatty acid signatures of pelagic prey. Elevated levels of arachidonic acid in a benthivorous species suggested a minor dietary contribution of rhodophytes. The lack of larger taxa that undergo diel vertical migrations in the fish guts suggests that it is horizontal fluxes of non-, or weakly migrating zooplankton that are the main food supply to the resident fish consumers. Overall, there was no unambiguous support for the trophic blockage hypothesis. Differences in gut contents, trophic position and storage lipid fatty acid signatures of zooplanktivorous fishes indicate some degree of resource partitioning with respect to feeding habitats, prey selection and ontogenetic diet shifts. Irrespective of body size and feeding mode, the benthopelagic fishes occupied intermediate trophic positions between the 3rd and 4th trophic level in a food web composed mainly of omnivorous species.


Seamounts are often associated with dense aggregations of benthopelagic fishes (Rogers 1994; Koslow 1997; Koslow et al. 2000; Clark 2001; Dower & Perry 2001). Several hypotheses have been developed to explain how these standing stocks are sustained. The hypothesis of locally enhanced autochthonous seamount production (Uda & Ishino 1958) states that a local increase in primary production, due to seamount-induced upwelling of nutrients and retention of particles in Taylor columns, would promote the growth of local zooplankton populations that could sustain resident fish stocks. Although elevated chlorophyll concentrations have been occasionally observed above seamounts, they generally do not persist long enough to affect local zooplankton stocks (reviewed by Genin & Dower 2007). The sound-scattering layer interception hypothesis (Isaacs & Schwartzlose 1965) states that increased food supply to the seamount fauna results from topographic blockage and trapping of the vertically migrating fauna of the sound-scattering layer during descent. It is essentially a trophic blockage hypothesis and was suggested as a possible mechanism to maintain fish aggregations at seamounts (Rogers 1994; Koslow 1997; Parin et al. 1997; Genin 2004). Enhanced flux of prey organisms past the seamounts from adjacent oceanic regions due to the amplification of near-bottom flows has also been suggested as an important mechanism to sustain the resident seamount fauna (Tseitlin 1985; Genin et al. 1988; Koslow 1997; Genin 2004). Increased food supply might also result from behavioural responses of zooplankton to vertical water mass movement when zooplankton swim vertically to maintain their depth and become locally aggregated (Genin 2004).

Biochemical markers, such as stable isotopes and fatty acids, have been used extensively in the study of marine food webs (e.g.Iken et al. 2001, 2005; Davenport & Bax 2002; Dalsgaard et al. 2003; Iverson et al. 2004). In contrast to gut content analyses, biochemical markers provide time-integrated signals of assimilated food. Isotopic signatures can be used to evaluate carbon sources and the trophic position of organisms (e.g.Peterson & Fry 1987; Vander Zanden & Rasmussen 2001; Post 2002), while fatty acid biomarkers indicate predator–prey relationships for broad taxonomic groups of prey (Dalsgaard et al. 2003 and references therein). In this study, fatty acid signatures of the neutral lipid fractions were used for trophic analysis. The fatty acid profiles of neutral lipids, which are used for energy storage, are more variable and more readily influenced by dietary input than the conservative fatty acid composition of the structural lipids (mainly phospholipids) of a consumer (Sargent & Henderson 1995).

The benthopelagic fish species analysed in this study are part of a trawl survey conducted on the summit plateau of Seine Seamount (Christiansen et al. 2009). A combined approach of gut content and biochemical marker analyses was used to investigate the food sources, nutritional pathways and trophic interactions of the benthopelagic fish assemblage; our specific objectives were to (i) identify the diet of fishes and their trophic interactions on the summit of Seine Seamount; and (ii) test the trophic blockage hypothesis as a mechanism to sustain fish consumers on the seamount.

Material and Methods

Study area

Seine Seamount is located northeast of Madeira (33°50′ N–14°20′ W) within the oligotrophic regime of the eastern North Atlantic Subtropical Gyre (NASE) biogeochemical province as defined by Longhurst (1995, 1998) (Fig. 1). It is a single summit, cone-shaped seamount which rises from more than 4000 m depth to a summit plateau at ∼170 m. The summit plateau is dominated by coarse biogenic sediments with few outcropping rocks; the presence of ripple marks indicates strong bottom currents (Christiansen, unpublished data).

Figure 1.

 Location and bathymetry of Seine Seamount. Sampling locations of the fish trawls are indicated for December 2003 (broken line), March 2004 (solid line) and May 2005 (solid grey lines). POM water sample locations (filled circles) and MOCNESS zooplankton haul locations (arrows) are given for the survey of March 2004.


Benthopelagic fishes were sampled on the summit plateau of Seine Seamount at water depths of 170–190 m during three field surveys in December 2003, March 2004 and May 2005 (Fig. 1). Animals were collected during the day using an epibenthic sledge (December 2003), ottertrawls with a footrope length of about 15 m (March 2004) and 25 m (May 2005), and a 2-m beamtrawl (May 2005). Samples for particulate organic matter (POM), zooplankton and micronekton were collected during the survey in March 2004 at locations above the summit and slopes of Seine Seamount (Fig. 1).

A total of 16 benthopelagic fish species were caught during the surveys and catches were dominated by the snipefish Macroramphosus spp., with Capros aper, Centracanthus cirrus and Anthias anthias being the next most abundant species (Christiansen et al. 2009). Ten of these species were used for trophic analyses and represented four feeding types: benthivores, primarily zooplanktivores, primarily piscivores and species with mixed crustacean/cephalopod/fish diets (Table 1).

Table 1.   Summary of samples of benthopelagic fish species collected on the summit plateau of Seine Seamount.
orderfamilyspeciessampling periodfeeding typetotal length mean (range)nGutnSInLip
  1. Feeding type abbreviations are according to the literature (superscript a–i); B = benthivore; Z = zooplanktivore; P = piscivore; M = mixed crustacean/cephalopod/fish diet. Total fish length (cm) is given as the mean with ranges. juv. = juvenile; nGut = number of fish guts analysed; nSI = number of individuals sampled for stable isotope analysis; nLip = number of individuals sampled for lipid analysis. Feeding type source data: (a) Whitehead et al. 1986; (b) Halpern & Floeter 2008; (c) Fock et al. 2002a; (d) Matthiessen et al. 2003; (e) Lopes et al. 2006; (f) FishBase 2009, (g) Morato et al. 1999; (h) O’Sullivan et al. 2004; (i) Ehrich 1974.

PleuronectiformesBothidaeArnoglossus rueppelliDec 03Ba,b11.8 (10.5–14.5)633
SyngnathiformesCentriscidaeMacroramphosus spp.Dec 03Za,c,d,e11.4 (11.0–11.7)333
Macroramphosus spp.Mar 0412.5 (11.0–14.0)16225
Macroramphosus spp. juv.Mar 047.3 (6.5–8.0)622
ZeiformesCaproidaeCapros aperMar 04Za,c,e11.6 (9.0–14.5)20205
PerciformesSerranidaeAnthias anthiasMar 04Za18.5 (16.0–20.0)6103
CentracanthidaeCentracanthus cirrusMar 04Zb19.4 (18.5–20.0)6102
Centracanthus cirrus juv.Mar 048.0 (7.5–8.5)683
CarangidaeTrachurus picturatusMar 04Ma,i38.5 (37.0–41.0)444
Trachurus picturatusMay 0538.7 (38.0–39.5)33
ScorpaeniformesScorpaenidaePontinus kuhliiMay 05Mf25.1 (19.0–32.5)6
AnguilliformesCongridaeConger congerMay 05Pg,h122 (104–146)4
ScopeliformesAulopidaeAulopus filamentosusMay 05Mf38.5 (36.0–41.0)2
TorpediformesTorpedinidaeTorpedo nobilianaMay 05Pa69.5 (52.0–87.0)2

Tissue samples were dissected from the dorsal muscle of benthopelagic fish species directly after recovery from the trawls and were stored at −20 °C for stable isotope and at −80 °C, or in liquid nitrogen, for lipid analysis. Total length of all specimens was recorded and the catch preserved in borax-buffered formalin. In the laboratory, guts of the tissue-sampled individuals were dissected. Additional muscle tissue samples for stable isotope analysis were dissected from formalin-preserved specimens together with reference samples from individuals that had been tissue-sampled prior to formalin preservation. Fishes caught during the survey in May 2005 were frozen whole at −20 °C and muscle samples were dissected from the frozen specimens after return to the laboratory.

Water samples for stable isotope analyses of POM were collected at 50 m depth using Niskin bottles mounted on a CTD rosette. Prior to filtration, the samples were passed through a 300-μm mesh size sieve to remove larger zooplankton. Water samples (10 l per filter) were vacuum-filtered on board at low pressure on pre-combusted (450 °C; 5 h) GF/C filters. Filters were wrapped in muffled aluminium foil (450 °C; 5 h) and stored at −20 °C until further analysis.

Zooplankton and micronekton were sampled using a Double-MOCNESS (Wiebe et al. 1985) with a 1-m2 opening and equipped with 20 dark-coloured nets of 333-μm mesh size. Sampling depths covered the upper 150 m above the summit (from ∼20 m above the seafloor), and the upper 600 m above the slopes of the seamount to include diel vertically migrating species at their depth range during day hauls. Specimens for stable isotope and lipid analyses of selected species were sorted on board using a dissecting microscope. Depending on the body size of a species, each sample consisted of 1–200 individuals. Stable isotope samples were stored at −20 °C and lipid samples in liquid nitrogen.

Laboratory analysis

Gut contents

Prey items in fish guts were identified to the lowest possible taxonomic level and their size measured. The percentage frequency of occurrence (%FO) and percentage contribution to the total number of prey (%N) were determined for each prey group. The length of benthic polychaetes represents a minimum size as individuals were fragmented and fragment size was used as the best size estimate.

Stable isotopes

For the analysis of carbon and nitrogen isotopic ratios (δ13C and δ15N), frozen samples were lyophilised for at least 48 h. Isotopic compositions of the POM filter samples were measured in a Thermo-Finnigan Delta Plus Advantage mass spectrometer coupled to a Costech EAS Elemental Analyser at the UCSB/MSI Analytical Laboratory (analytical error ≤0.25‰). Lipids of lyophilised samples of benthopelagic and mesopelagic fishes were removed prior to isotopic analysis using Soxhlet extraction with a dichloromethane:methanol mixture (DCM:MeOH 2:1, v:v) for 4–6 h (Bligh & Dyer 1959). Afterwards, the samples were lyophilised again (48 h) and ground to a homogeneous powder with a mortar and pestle. Lipids of invertebrate zooplankton and micronekton samples were not removed to avoid loss of biomass of the often very small sample quantities. Instead, taking C:N as a proxy for lipid content, lipid-normalised values of δ13C were calculated according to Post et al. (2007): Δδ13C = −3.32 + 0.99 × C:N. Inorganic carbonates were removed from calcareous zooplankton samples (ostracods, pteropods) by adding 1 mol·l−1 hydrochloric acid (HCl) drop-by-drop to each powdered sample until CO2 release stopped (Jacob et al. 2005). The samples were dried at 60 °C and ground to homogeneous powder again. Stable isotope ratio and C:N analyses were performed simultaneously in a Thermo/Finnigan MAT Delta Plus mass spectrometer coupled to a Thermo NA 2500 Elemental Analyser via a Thermo/Finnigan Conflo II- interface at the GeoBio-CenterLMU (analytical error <0.15‰). Trophic levels (TL) were estimated using the mean δ15N of POM as baseline and an increase of 3.4‰ per trophic level (Minagawa & Wada 1984). The δ13C values were used to evaluate carbon sources due to small trophic shift of this ratio, which ranges from 0.3 to 1.3‰ depending on tissue type and species (McCutchan et al. 2003).

Additional muscle tissue samples for stable isotope analysis were taken from formalin-preserved specimens of four benthopelagic fish species (Table 2). To evaluate possible shifts in isotope ratios due to preservation, we compared samples before and after formalin treatment. For most species, formalin-preserved samples had slightly higher δ15N values (0.24–0.43‰) and lower δ13C values (1.31–1.54‰). These preservation effects were in the range of values reported in other studies (Bosley & Wainright 1999; Kaehler & Pakhomov 2001; Arrington & Winemiller 2002; Sarakinos et al. 2002; Koppelmann et al. 2009) and were significant for all species and juvenile stages investigated (P < 0.05; paired t-test), except for δ15N values of adult Macroramphosus spp. and juvenile Centracanthus cirrus (Table 2). Stable isotope ratios of formalin-preserved samples were, thus, corrected for preservation effects prior to data analysis.

Table 2.   Sample preservation effects on isotopic values of fish muscle tissue.
speciesnδ15N (‰)δ13C (‰)
  1. Mean δ15N and δ13C values of samples from the same individuals preserved frozen (−20 °C) and in 4% borax-buffered formaldehyde-seawater solution are listed with mean preservation-related isotopic differences (Δ); standard deviations are given in brackets. P values refer to paired t-test: **P < 0.01, *P < 0.05 and NS = not significant.

Macroramphosus spp.59.57 (0.33)9.70 (0.46)0.12 (0.17)NS−19.31 (0.10)−20.61 (0.09)−1.31 (0.12)**
Capros aper69.09 (0.41)9.33 (0.37)0.24 (0.15)*−19.25 (0.44)−20.59 (0.45)−1.35 (0.33)*
Centracanthus cirrus39.37 (0.26)9.80 (0.20)0.43 (0.08)*−18.75 (0.22)−20.29 (0.05)−1.54 (0.17)**
Centracanthus cirrus juv.38.50 (0.58)8.74 (0.81)0.24 (0.23)NS−20.05 (0.47)−21.52 (0.32)−1.47 (0.18)**
Anthias anthias39.80 (0.11)10.22 (0.10)0.42 (0.03)**−18.77 (0.21)−20.26 (0.11)−1.49 (0.14)**


Lipids were extracted from lyophilised fish and zooplankton samples with minor modifications as described by Hagen (2000) using ultrasonic disruption in a dichloromethane (DCM):methanol (MeOH) (2:1, v:v) mixture and a washing procedure with aqueous KCl solution (0.88%). To quantify fatty acids, a known amount of internal standard (nonadecanoic acid) was added to the sample prior to extraction. Total lipid extracts of the benthopelagic fish species were separated into lipid classes by solid phase extraction using 1 ml SiOH glass columns (CHROMABOND®, Macherey - Nagel (Internet Company)) on a vacuum manifold according to Peters et al. (2006). The neutral lipid fraction was eluted with a solvent sequence of hexane:diethylether (95:5 and 1:1, v:v).

Fatty acids of the neutral lipid fraction of the benthopelagic fish species and of the total lipids of zooplankton samples were converted to methyl esters by transesterification with methanol containing 3% concentrated sulphuric acid at 80 °C for 4 h (Kattner & Fricke 1986). After cooling, 4 ml of bi-distilled water was added, and fatty acid methyl esters (FAME) were extracted three times with 2 ml hexane.

The FAMEs were separated and quantified using an Agilent 6890N gas chromatograph equipped with a DB-WAX column (30 m length × 0.32 mm inner diameter, 0.25 μm film thickness) operated with a temperature program and helium as carrier gas. Samples were injected using a temperature-programmed vaporiser injector (Gerstel® CIS3, Mühlheim a. d. Ruhr, Germany) in solvent vent mode. The FAMEs were detected by flame ionisation and identified by comparing retention times with those obtained from standards and/or from the literature. Total fatty acids were calculated as the sum of all identified fatty acids from the chromatogram.


Gut contents

A total of 4316 prey items were identified in 36 categories (Table 3). The guts of the four zooplanktivorous species (Centracanthus cirrus, Macroramphosus spp., Capros aper and Anthias anthias) contained almost exclusively (96–100%) small-sized (1–2 mm) prey items, irrespective of predator size (Table 3). Copepods were the dominant prey, with oncaeid and calanoid copepods being the dominant groups. Oncaeids were generally more abundant in the guts than calanoids, except for the more pelagic-living C. cirrus, which had more calanoids in its guts. Of those 11 calanoid taxa identified to a lower taxonomic level, the only species that performs strong diel vertical migrations, Pleuromamma spp., occurred at low frequency and abundance. The most frequent and abundant non-copepod crustacean prey items were ostracods. Centracanthus cirrus and Macroramphosus spp. consumed the largest range of prey categories, which included euphausiid furcilia and calyptopis larvae, mysids, decapods and amphipods, and non-crustacean pelagic invertebrate prey, such as chaetognaths, polychaetes and gastropods in low abundances. Foraminiferans frequently occurred in the guts of Macroramphosus. Benthic prey items, which consisted of benthic polychaetes, were present in 70% of the guts of C. aper and occasionally occurred in the guts of Macroramphosus spp.

Table 3.   Prey consumed by the benthopelagic fish species on the summit plateau of Seine Seamount expressed as percentage frequency of occurrence (%FO) and percentage of total number of prey items (%N).
prey categoryprey size range (mm)Arnoglossus rueppelliaCapros aperMacroramphosus spp.Centracanthus cirrusAnthias anthiasTrachurus picturatus
  1. Total numbers of fish guts analysed and total number of prey items are given at the bottom of the species columns (Totals). aSampled in December 2003, bsampled in December 2003 and March 2004, all others sampled in March 2004. cNot included in calculations of %N. n.q. = not quantified.

  Oncaeidae1–1.5  10059.68962.25029.410012.310051.410052.9  
  Corycaeidae1–2  200.6422.7  671.6331.6172.2  
  Sapphirinidae1–2    50.5          
  Harpacticoidea1    110.36735.3170.01008.8    
  Oithonidae1  50.1    170.1      
   Unident. Calanoida1–4  9034.35311.05035.310061.310037.110037.9  
   Candacia sp.2–4  200.7160.7  670.5  170.6  
   Pleuromamma sp.1–2174.550.1160.5  831.1      
   Euchaeta sp.1.5–2.5  50.250.2  831.0      
   Lucicutia sp.1.5–2  50.250.5  1003.6      
   Clausocalanus sp.1–1.2    215.9  10013.2  174.1  
   Rhincalanus nasutus3–4  150.450.2  1000.5      
   Nannocalanus sp.2.1–2.5    111.3  500.2      
   Neocalanus sp.2        170.2      
   Temora sp.2    50.2          
   Aetideidae1.8–2        500.2      
   Scolecithricidae2        330.4      
 Ostracoda0.5–1.5  301.9429.7  1002.6331.0502.2  
 Mysidacea7–105013.6  111.0          
 Euphausiacea, Furc. & Calyp.1–4.5    52.0  830.6      
 Decapoda2–10179.1      170.0      
 Amphipoda4    50.2  170.0      
 Unident. Crustacea pieces 6718.2  50.3          
 Unident. Foram. fragmentsc0.5–1    42n.q.          
 Gastropoda, pelagic1–2    50.3          
 Unident. Chaetognatha4–6        170.1      
 Polychaeta, pelagicca. 3        500.4      
 Polychaeta, benthicca. 6–208354.5701.7110.3          
 Macroramphosus spp. juv.60–75              75100
 Fish eggs1        170.0      
 Fish scalesc   10           25 
 Shell fragments 17   5           
 Echinoderm remains     5           
 Sand grains 17   5           
  No. guts (n)No. prey itemsNo. guts (n)No. prey itemsNo. guts (n)No. prey itemsNo. guts (n)No. prey itemsNo. guts (n)No. prey itemsNo. guts (n)No. prey itemsNo. guts (n)No. prey itemsNo. guts (n)No. prey items
Totals 62220805195986176215863856314417

Ontogenetic differences in the gut contents were apparent for Macroramphosus spp. and C. cirrus (Table 3), although results for Macroramphosus juveniles need to be treated with caution due to the low number of prey items present in the guts. Compared to their adult congeners, the guts of juveniles contained smaller and less diverse prey. Proportions of the main copepod groups also differed markedly, as Macroramphosus juveniles contained fewer oncaeids and more calanoids than the adults; this pattern was reversed in C. cirrus.

The gut contents of the benthivorous flatfish Arnoglossus rueppelli were dominated by benthic polychaetes and non-copepod crustaceans such as mysids, decapods and unidentified crustacean fragments (Table 3). Stomach contents of the blue jack mackerel Trachurus picturatus consisted exclusively of fish remains, mainly juvenile Macroramphosus spp. (Table 3).

Stable isotopes

The δ13C values of the 10 benthopelagic fish species studied covered a range of 4‰ (−20.8 to −16.8‰; Table 4, Fig. 2). Juvenile zooplanktivores had the lowest δ13C values, while those of the piscivorous electric ray Torpedo nobiliana were the most enriched. However, the interquartile range (IQR = 0.7‰) of δ13C values for all fishes was much narrower. When the markedly enriched δ13C values of T. nobiliana were excluded, the fishes covered a total δ13C range of only 2.6‰ irrespective of feeding mode, indicating a common food source. The average δ13C value of pelagic copepods, which constituted the major prey of zooplanktivores, was depleted by about 1.5–2‰ compared to the average δ13C values of adult zooplanktivores (Fig. 2). For piscivorous fish species, a trophic shift in δ13C of about 1.6‰ was observed between Trachurus picturatus and its main prey Macroramphosus juveniles, and of about 1‰ between Conger conger and its main prey Capros aper and Macroramphosus scolopax (Fig. 2). There was no difference in the carbon isotope signals between migrating and non-migrating taxa. Carbon isotope values of the myctophid fish species were in the lower range of those found for juvenile zooplanktivores. Although POM represents the base of the pelagic food web, its δ13C values were markedly depleted compared to those of pelagic consumers (Fig. 2), which is most likely caused by the lack of correction for lipid content of the POM samples, as lipids result in depleted δ13C values (Post et al. 2007).

Table 4.   Summary of δ13C and δ15N signatures of benthopelagic fish species collected on the summit plateau of Seine Seamount.
speciessampling periodnδ13C (‰)δ15N (‰)
mean ± SDrangemean ± SDrange
  1. Species that include samples corrected for formalin preservation effects are marked with a superscript b when both δ13C and δ15N were corrected, and with a superscript a when only δ13C values were corrected (see Methods for details).

Arnoglossus rueppelliDec 033−18.86 ± 0.11−18.94 to −18.739.06 ± 0.039.04–9.09
Macroramphosus spp.Dec 033−19.21 ± 0.39−19.55 to −18.789.79 ± 0.219.62–10.03
Macroramphosus spp.aMar 0422−19.41 ± 0.17−19.71 to −19.119.54 ± 0.278.88–10.00
Macroramphosus spp. juv.Mar 042−19.99−20.06 to −19.917.687.61–7.75
Capros aperbMar 0420−19.34 ± 0.29−19.70 to −18.629.01 ± 0.438.29–9.81
Anthias anthiasbMar 0410−18.87 ± 0.15−19.12 to −18.639.69 ± 0.179.39–9.91
Centracanthus cirrusbMar 0410−18.75 ± 0.19−19.00 to −18.399.48 ± 0.179.13–9.77
Centracanthus cirrus juv.aMar 048−20.25 ± 0.38−20.83 to −19.528.51 ± 0.617.66–9.46
Trachurus picturatusMar 044−18.41 ± 0.13−18.50 to −18.2310.38 ± 0.1410.24–10.52
Trachurus picturatusMay 053−19.02 ± 0.21−19.22 to −18.809.79 ± 0.709.12–10.51
Pontinus kuhliiMay 056−18.73 ± 0.16−18.88 to −18.4610.26 ± 0.469.68–10.82
Aulopus filamentosusMay 052−19.00−19.05 to −18.9410.7510.54–10.96
Torpedo nobilianaMay 052−16.99−17.23 to −16.7510.6110.43–10.79
Conger congerMay 054−18.41 ± 0.21−18.61 to −18.1711.27 ± 0.3510.79–11.55
Figure 2.

 Mean δ13C values and ranges of benthopelagic fish species and potential pelagic food sources. Fish species sampled during the three surveys are marked according to sampling time: light grey = December 2003, black = March 2004 and dark grey = May 2005. Symbols for the benthopelagic fish species refer to feeding types (bsl00072 = benthivore; • = zooplanktivore; bsl00066 = piscivore; bsl00001 = mixed crustacean/cephalopod/fish diet). Mean values and ranges of pelagic food sources (○), with number of samples measured given in brackets, were determined from samples collected in March 2004. Crossed circle symbols denote species with strong diel vertical migration (DVM). A Strongly migrating euphausiid species: Euphausia hemigibba (n = 4), Thysanopoda aequalis (n = 2). B Non- or weakly migrating euphausiid species: Nematoscelis spp. furcilia (n = 1), Nematoscelis atlantica (n = 3), Thysanoessa sp. (n = 1).

The potential pelagic food items of the benthopelagic fishes covered a total δ15N range of 6.8‰ between the first and third trophic level (Fig. 3). Copepods, which constituted the dominant prey item for all zooplanktivores based on gut contents, covered nearly the total range of δ15N values measured for potential prey items. Calanoids generally occupied higher trophic positions than oncaeids. Taxa that undergo pronounced diel vertical migrations (i.e. copepods, euphausiids, pteropods) had δ15N values in the same range as those found in non- or weakly migrating zooplankton taxa; δ15N values of myctophids, which have substantial vertical migrations, were similar to juvenile zooplanktivores.

Figure 3.

 Mean δ15N values and ranges of benthopelagic fish species and potential pelagic food sources. Trophic levels (TL) were estimated using the mean δ15N value of POM as baseline (TL1) and an increase of 3.4‰ per trophic level. Fish species sampled during the three surveys are marked according to sampling time: light grey = December 2003, black = March 2004 and dark grey = May 2005. Symbols for the benthopelagic fish species refer to feeding types (see Fig. 2). Mean values and ranges of pelagic food sources (○), with number of samples measured given in brackets, were determined from samples collected in March 2004. Crossed circle symbols denote species with strong diel vertical migration (DVM). A Strongly migrating euphausiid species: Euphausia hemigibba (n = 4), Thysanopoda aequalis (n = 2). B Non- or weakly migrating euphausiid species: Nematoscelis spp. furcilia (n = 1), Nematoscelis atlantica (n = 3), Thysanoessa sp. (n = 1).

In contrast to the large range of δ15N values occupied by potential pelagic prey, the δ15N values of the benthopelagic fishes spanned 3.9‰, ranging from 7.6‰ in juvenile Macroramphosus spp. to 11.6‰ in C. conger (Table 4, Fig. 3). Trophic position, calculated from the average δ15N values, increased from juvenile zooplanktivores, via adult zooplanktivores and the benthivorous flatfish species, to those species with a mixed diet of fish/cephalopods/crustaceans or those which consume mostly fish. Assuming that the mean δ15N value of POM represents the first trophic level, trophic positions of the fishes studied by us fell between the 3rd and 4th trophic level, the exception being juvenile zooplanktivores, which apparently fed just below the 3rd trophic level (Fig. 3). Muscle δ15N values increased with body size (rS = 0.678, P < 0.01, n = 99).

Temporal differences in stable isotope signatures (δ13C and δ15N) were tested for Macroramphosus spp. sampled in December 2003 and March 2004, and for T. picturatus sampled in March 2004 and May 2005. Significant temporal differences were only detected for δ13C values of T. picturatus (P < 0.05, t-test), which were on average 0.61‰ higher in March 2004.

Fatty acid signatures

The storage lipid fatty acid profiles analysed for six benthopelagic fish species were dominated by the saturated fatty acids 16:0 and 18:0, the unsaturated phytoplankton marker fatty acids 16:1(n-7), 20:5(n-3) and 22:6(n-3), and the marker fatty acid for carnivorous zooplankton 18:1(n-9) (Appendix S1, Fig. 4A). Inter- and intra-specific variability in the proportions of the most abundant fatty acids were generally small, except for the poly-unsaturated fatty acid 22:6(n-3) and variable proportions of arachidonic acid 20:4(n-6) in the storage lipids of Arnoglossus rueppelli (Fig. 4A). Temporal differences in fatty acid composition between individuals of Macroramphosus spp. sampled in December 2003 and March 2004, and individuals of Trachurus picturatus sampled in March 2004 and May 2005, were also generally small and within the range of intraspecific variability (Appendix S1).

Figure 4.

 Proportions of the most abundant unsaturated fatty acids (FA) in (A) the total storage lipids (NL = neutral lipids) of the benthopelagic fish species, and (B) the total lipids (TL) of potential pelagic food sources for the benthopelagic fishes on Seine Seamount. Values for benthopelagic fish species and stages are presented as means and ranges from the three surveys. Mean values and ranges of potential pelagic food sources (number of samples in brackets) were determined from samples collected in March 2004. Potential prey species with strong diel vertical migration (DVM) are indicated by grey-coloured bars. A Non- or weakly diel vertically migrating calanoid copepod species: Lucicutia spp. (n = 2), Clausocalanus spp. (n = 1), Euchaeta spp. (n = 2). B Strongly diel vertically migrating calanoid copepod species: Pleuromamma xiphias (n = 4), C Strongly diel vertically migrating euphausiid species: Euphausia hemigibba (n = 3) D Mysidacea (n = 1), Ostracoda (n = 1). E Chaetognatha (n = 1), Fish eggs (n = 2), Myctophidae larvae (n = 2).

Principal component analysis (PCA) on the eight most abundant storage lipid fatty acids of the benthopelagic fish species extracted three components with eigenvalues >1, of which the first two explained 74% of the variance (Fig. 5). Despite considerable overlap in fatty acid composition, some degree of separation between species and stages was apparent. PC1, which explained 49% of the variance, separated species and stages along a benthic–pelagic gradient. Adults and juveniles of Centracanthus cirrus and juveniles of Macroramphosus spp. were characterised by higher proportions of pelagic marker fatty acids, whereas the benthivorous A. rueppelli had elevated proportions of the assumed benthic marker fatty acid 20:4(n-6). Arachidonic acid 20:4(n-6) separated A. rueppelli from the other species along the PC2. The zooplanktivore species centrally positioned in the plot strongly overlapped in their fatty acid composition, indicating a high degree of similarity in their food sources. PC1 and PC2 separated individuals of the piscivorous T. picturatus from other feeding types by a weak diatom signal in concert with high proportions of the poly-unsaturated fatty acid 22:6(n-3), which is a dominant component of biomembranes and generally abundant in fish lipids.

Figure 5.

 Principal component analysis on the relative fatty acid compositions of the most abundant storage lipid fatty acids of the benthopelagic fish species on Seine Seamount. Species labeled with an asterisk (*) refer to specimens sampled in December 2003, and those marked with an apostrophe (‘) to those sampled in May 2005; all other specimens were sampled in March 2004; filled circles = fatty acids; scales were adjusted to combine plots: scales of principal components (PC) refer to sample plot, scale of variables ranges from −1 to +1 for both PCs. Proportion of variance accounted for by each PC is given in brackets.

The fatty acid signatures of the total lipids of potential pelagic prey were largely similar among taxonomic groups, except for oncaeid copepods, which differed markedly in mean proportions of nearly all of the abundant fatty acids (Fig. 4B): they had higher proportions of 18:1(n-9) and reduced proportions of 22:6(n-3) and 20:5(n-3). Fatty acid signatures of zooplankton and myctophids did not differ between taxa who perform large vertical migrations and those which do not.

The fatty acid signatures of total lipids of potential pelagic prey taxa were very similar to those of storage lipids of the benthopelagic fish species (Fig. 4A,B). The assumed benthic marker fatty acid 20:4(n-6) was low in pelagic taxa and in fish, except for the flatfish species. Despite pronounced differences in the fatty acid composition of oncaeid and calanoid copepods, zooplanktivorous fish that preferentially fed on either copepod group, based on gut content analysis, did not differ significantly in fatty acid profiles.


Primary food sources of the benthopelagic fishes

The benthopelagic fish species studied had a narrow range of δ13C values that matched those of pelagic prey items, suggesting a common pelagic food source irrespective of the feeding mode of the fish consumers. Gut contents of the zooplanktivorous species, which consisted mainly of pelagic copepods, supported the trophic importance of pelagic prey for fishes, based on isotope markers. A nutritional link to epipelagic phytoplankton was also indicated by a high degree of similarity between the fatty acid signatures of the benthopelagic fishes and their potential pelagic prey, which were dominated by marker fatty acids for dinoflagellates [22:6(n-3)], diatoms [16:1(n-7), 20:5(n-3)] and carnivorous zooplankton [18:1(n-9); e.g.Dalsgaard et al. 2003].

Minor dietary contributions from benthic sources were possible. Benthic prey, mainly polychaetes, was recorded in the guts of the flatfish Arnoglossus rueppelli. The storage lipids of this species were characterised by higher proportions of arachidonic acid 20:4(n-6), an essential fatty acid that is abundant in rhodophytes (Pettitt et al. 1989; Khotimchenko et al. 1990; Dembitsky et al. 1991; Dalsgaard et al. 2003). The recovery of coralline red algae from the summit plateau of Seine Seamount during the survey in May 2005 (Beck et al. 2005) confirmed the presence of benthic primary producers. However, the contribution of macroalgae to fish diets was likely to be minor due to low abundances of macroalgae and low light levels at the summit. Elevated δ13C values of the piscivorous electric ray Torpedo nobiliana compared to the other benthopelagic fish species also indicated a possible dietary contribution of benthic macroalgae, which can have enriched δ13C values (Moncreiff & Sullivan 2001; Behringer & Butler 2006; Jaschinski et al. 2008), or of benthic diatoms (Kang et al. 2003; Riera & Hubas 2003); some epibenthic invertebrates on Seine Seamount summit were also enriched in 13C (Hirch et al., unpublished data).

Evidence for the sound-scattering layer interception hypothesis?

The sound-scattering layer interception hypothesis proposed by Isaacs & Schwartzlose (1965) predicts enhanced food supply to consumers on seamounts due to topographic blockage of diel vertical migrators during their descent. It predicts that this effect is highest for seamounts at intermediate depths, where the summit is just below the photic layer (Genin 2004). The summit plateau of Seine Seamount at about 170 m depth is situated just below the photic layer (∼130–150 m; Beck et al. 2005) and the resident benthopelagic fish fauna was, thus, expected to receive food supply through the trapping of diel vertical migrators. Studies on the summit plateau of the Great Meteor Seamount (summit depth ∼280 m), situated southwest of Seine Seamount, reported high daytime abundances of vertically migrating zooplankton taxa close to the seafloor of the plateau (Martin & Nellen 2004). The distribution and diel behaviour of the benthopelagic fish assemblage were interpreted to reflect food supply through the topographic blockage mechanism (Fock et al. 2002a,b).

Based on gut contents of the benthopelagic fishes examined, we did not find support for a major trophic pathway consistent with the topographic blockage mechanism. Zooplanktivorous fish species fed predominantly on small (<0.5 cm), presumably non- or weakly migrating copepods and contained very few individuals of zooplankton taxa that undertake diel vertical migrations. Migrating zooplankton also had no dietary importance for the benthivore flatfishes. Similarly, the guts of the piscivore Trachurus picturatus contained no diel vertically migrating micronekton such as myctophids.

We may have underestimated the contribution of migrating taxa to the diet of benthopelagic fishes due to the small number of stomachs analysed. However, body sizes of prey items in the gut contents of fishes largely reflected the size distributions of zooplankton reported for the water column above the summit plateau (Martin & Christiansen 2009). Zooplankton biomass above the summit plateau was dominated by small (<0.5 cm) non-vertically migrating copepods. Larger (>0.5 cm) zooplankton that undergo diel vertical migrations were nearly absent at all times, despite being abundant above the seamount slopes and at a reference site outside the sphere of influence of the seamount (Martin & Christiansen 2009). Low numbers of diel vertical migrators above the summit may be due to predation by pelagic zooplanktivores, such as pelagic fishes or gelatinous zooplankton. Gap formation above the seamount during the night might be caused by current-driven displacement.

Because larger zooplankton that undertake diel vertical migrations are rare above the summit plateau of Seine Seamount and in the guts of zooplanktivores, topographic trapping is likely to be of very minor trophic importance. Rather, benthopelagic fish consumers rely more on current-driven horizontal fluxes of small planktonic prey.

Resource partitioning among zooplanktivores

Despite considerable dietary overlap among the benthopelagic zooplanktivorous fishes, differences in gut contents, storage lipid fatty acid signatures and trophic position indicated some degree of resource partitioning with respect to feeding habitats, prey selection and ontogenetic diet shifts. Habitat, prey and time have been proposed as the most important environmental niche dimensions for niche differentiation (Schoener 1974), which is generally thought to reduce competition and promote species co-existence (e.g.Hayward & McGowan 1979; Hopkins & Sutton 1998).

Resource partitioning through differences in the vertical feeding position was suggested by gut contents and fatty acid biomarkers and is supported by studies on the distribution of fish species at seamounts (Ehrich 1974; Kukuev 2004; Pakhorukov 2008). Near-bottom fish species had higher proportions of oncaeid copepods in their stomachs, whereas calanoid copepods were more abundant in the diet of the more pelagic C. cirrus. There was some evidence, based on fatty acid markers, for vertical segregation in feeding: more pelagic-living species and juveniles had higher amounts of fatty acids typical of phytoplankton and zooplankton and lower amounts of the benthos-associated fatty acid 20:4(n-6). Resource partitioning through differences in prey choice in zooplanktivores has been reported for fishes on seamounts (Fock et al. 2002a). We found that zooplanktivore species differed in their proportions of crustacean prey groups and of non-crustacean prey which they consumed, and the extent to which they utilized benthic food items. Juveniles and adults of Macroramphosus spp. and C. cirrus also showed some degree of trophic segregation. Juveniles had lower δ15N values, suggesting that they feed more on smaller, and presumably more herbivorous, copepods (Turner 2004).

Trophic structure of the benthopelagic fish community

Trophic positions, determined from δ15N values, of the benthopelagic fish species differed between feeding types and increased with body size. Juvenile zooplanktivores occupied the lowest trophic position. Adult zooplanktivores and the benthivorous flatfish were intermediate. Species with a mixed diet of fishes, cephalopods and crustaceans and piscivores fed at the highest trophic position for the guild sampled.

Positive correlations between body size and trophic level have been explained by ontogenetic diet shifts and by the general observation that predators are typically larger than their prey and thus trophic position often increases with body size within a given food web (France et al. 1998; Jennings et al. 2001; Jennings & Mackinson 2003). In this study, all fishes occupied a narrow range of trophic positions. Most species feed at intermediate trophic levels, and this could be explained by significant omnivory (Marguillier et al. 1997; France et al. 1998). The maximum trophic position (MTP) of 3.8 in this study, which was occupied by the conger eel Conger conger, was comparable to that reported for benthic invertebrates from seamounts on the Norfolk Ridge (MTP: 4–5; depth range: 200–900 m) and to those reported for other shallow and deep marine ecosystems (MTP: 3.5–4.5; Samadi et al. 2007). Compared to the 16 species collected during the bottom trawl catches on the summit plateau (Christiansen et al. 2009), catches from longline surveys (depth range: summit to 2000 m) of Seine Seamount consisted of a total of 41 fish species (Menezes et al. 2009) and contained higher proportions of large predator species such as sharks. Thus, it is plausible that the MTP of seamount fishes would have been higher had top predators been included in our analysis.

In contrast to the narrow range of δ15N values found in benthopelagic fishes, zooplankton and micronekton had markedly more variable nitrogen isotope signals. The narrower isotopic ranges in the zooplanktivores could be the result of time-integrated averaging of isotopic signals of assimilated prey rather than feeding on a narrow range of prey items.

The benthopelagic fish community on the summit plateau of Seine Seamount was energetically underpinned primarily by pelagic primary production, with only minor contributions from benthic primary producers (e.g. rhodophytes; Fig. 6). Major trophic pathways include consumption of pelagic copepods – advected to the seamount by horizontal currents – by zooplanktivores, and predation of these zooplanktivores by piscivorous species such as T. picturatus and C. conger. Benthivores, such as the flatfish A. rueppelli, are likely to be energetically supported by phytoplankton detritus assimilated by benthic invertebrates.

Figure 6.

 Conceptual diagram of main trophic pathways to the benthopelagic fish assemblage on the summit plateau of Seine Seamount. Pathways observed in this study are indicated by black arrows. Major pathways are depicted by solid, thick lines and minor ones by thin or broken lines. Trophic links taken from the literature are represented by grey arrows. Investigated fish species are listed according to their vertical habitat categories derived from Pakhorukov (2008), Kukuev (2004) and Ehrich (1974). Pelagic organisms that undertake pronounced diel vertical migrations (DVM) are denoted by cross-hatched boxes. Mechanisms that are hypothesized to supply pelagic food sources (POM, non- or weak DVM zooplankton) and processes which we postulated to explain the lack of DVM zooplankton in the overlying water column are illustrated in ellipses.


This research is part of the OASIS (OceAnic Seamounts: an Integrated Study) project, which was funded by the European Commission under the Fifth Framework Programme (contract EVK3-CT-2002-00073-OASIS). We thank the crews of the FS Meteor and FS Poseidon for their professional support at sea. We would like to thank Dr Robert Petty (University of California Santa Barbara, Marine Science Institute Analytical Laboratory) and Dr Ulrich Struck (GeoBio-Center, Ludwig-Maximilans-Universität, Munich) for running the stable isotope analyses.