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Keywords:

  • Dissostichus eleginoides ;
  • food web;
  • isotopic niche width;
  • methane seeps;
  • stable isotopes;
  • trophic level

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Appendix 1: Carbon and nitrogen isotopes ratios of heterotrophic macro and megafauna in the CMSA. Trophic positions are estimated by nitrogen isotope ratios and feeding modes according to indicated references

Studies of the trophic structure in methane-seep habitats provide insight into the ecological function of deep-sea ecosystems. Methane seep biota on the Chilean margin likely represent a novel biogeographic province; however, little is known about the ecology of the seep fauna and particularly their trophic support. The present study, using natural abundance stable isotopes, reveals a complex trophic structure among heterotrophic consumers, with four trophic levels supported by a diversity of food sources at a methane seep area off Concepción, Chile (~36° S). Although methanotrophy, thiotrophy and phototrophy are all identified as carbon fixation mechanisms fueling the food web within this area, most of the analysed species (87.5%) incorporate carbon derived from photosynthesis and a smaller number (12%) use carbon derived from chemosynthesis. Methane-derived carbon (MDC) incorporation was documented in 22 taxa, including sipunculids, gastropods, polychaetes and echinoderms. In addition, wide trophic niches were detected in suspension-feeding and deposit-feeding taxa, possibly associated with the use of organic matter in different stages of degradation (e.g. from fresh to refractory). Estimates of Bayesian standard ellipses area (SEAB) reveal different isotopic niche breadth in the predator fishes, the Patagonian toothfish Dissostichus eleginoides and the combtooth dogfish Centroscyllium nigrum, suggesting generalist versus specialist feeding behaviors, respectively. Top predators in the ecosystem were the Patagonian toothfish D. eleginoides and the dusky cat shark, Bythaelurus canescens. The blue hake Antimora rostrata also provides a trophic link between the benthic and pelagic systems, with a diet based primarily on pelagic-derived carrion. These findings can inform accurate ecosystem models, which are critical for effective management and conservation of methane seep and adjacent deep-sea habitats in the Southeastern Pacific.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Appendix 1: Carbon and nitrogen isotopes ratios of heterotrophic macro and megafauna in the CMSA. Trophic positions are estimated by nitrogen isotope ratios and feeding modes according to indicated references

Discovered in 1979 (Lonsdale 1979), cold seeps are now known to be common habitats along geologically active and passive continental margins worldwide, and are found from shelf depths to hadal trenches (Barry et al. 1996; Corselli & Basso 1996; Sibuet & Olu 1998; Sibuet & Olu-LeRoy 2002; Campbell 2006; Gracia et al. 2011). Like hydrothermal vents, cold seeps have been recognized as unique ecosystems that form hotspots of biological production and diversity in the deep sea (Sahling et al. 2003; Cordes et al. 2010a; Bernardino et al. 2012). In these environments, cold fluids enriched with hydrocarbons (e.g. methane), sulfide and other reduced compounds are emitted from the sea floor (Levin 2005) and are exploited by free-living and symbiotic microbes (e.g. methanotrophic and/or sulfur-oxidizing bacteria) (Orphan et al. 2004). Seep assemblages are commonly characterized by the presence of large chemosymbiotic megafauna (e.g. mytilid mussels, vesicomyid clams, vestimentiferan and frenulate polychaetes, gastropods and sponges) and by the presence of surficial bacterial mats (Sibuet & Olu 1998; Sibuet & Olu-LeRoy 2002; Levin & Mendoza 2007). Microbial production by bacteria and archaea at cold seeps forms the basis of complex benthic food webs, characterized by various energetic pathways and carbon sources (Brooks et al. 1987; Levin & Michener 2002; Carlier et al. 2010; Thurber et al. 2012). However, plankton detrital matter and terrestrially derived organic matter are also possible food sources for continental margin seep fauna (Levin et al. 2000; Levin 2005; Sellanes et al. 2008).

Stable isotopes can be a powerful tool to elucidate relative contribution of local productivity to the food web in chemosynthetic ecosystems (Van Dover & Fry 1989; Fisher et al. 1994; Levin & Michener 2002; Cordes et al. 2010b). The ratio of carbon (C13/C12) expressed as δ13C is used to identify the potential food sources at the base of the food web (DeNiro & Epstein 1978), and the δ15N values (N15/N14) are used to estimate the trophic position in heterotrophic organisms (Post 2002; McCutchan et al. 2003). At methane seeps, methane-derived carbon (MDC) is depleted in 13C relative to nearly all other energy sources, imparting a unique signature (δ13C ≤ −50‰) to organisms that graze upon free-living methanotrophic microbes or those that have methanotrophic symbionts (Childress et al. 1986; Fisher et al. 1987; Levin & Michener 2002). Extreme isotopic values are found among archaeal lipids, and these can be passed to consumers via sulfate-reducing bacteria that live in syntrophic partnership with methanotrophic archaea and carry out anaerobic methane oxidation (AOM; Elvert et al. 2003; Thurber et al. 2012). AOM yields hydrogen sulfide, which fuels carbon fixation by sulfide-oxidizing bacteria; δ13C values associated with sulfide oxidation can range from −21‰ to −37‰ for carbon fixed using Rubisco form I, and from −9 to −16‰ for carbon fixed using Rubisco form II (summarized in Levin & Michener 2002). However, δ13C values also depend on the CO2 signatures present in the environment (Lösekann et al. 2008), as well as the activity and amount of carbonic anhydrases present in the host and the symbionts (N. Dubilier pers. comm.). Photosynthesis-derived material typically has more 13C-enriched values (δ13C = −25 to −15‰) (Fry & Sherr 1984). These distinctions allow use of isotopic analysis to identify the carbon fixation pathway and the relative input of chemoautotrophic production. Moreover, chemosymbiotic animals from reducing areas often possess 15N-depleted values, potentially indicating inorganic nitrogen fixation or nitrate and ammonium assimilation (Conway et al. 1994; Thurber et al. 2010).

Recently discovered seep habitats in the SE Pacific offer an opportunity to study seep food webs in a different setting and biogeographic province. The Concepción Methane Seep Area (CMSA) was the first active methane seep explored off the Chilean coast (Sellanes et al. 2004, 2008). At the CMSA, symbiont-bearing seep fauna have been reported, including thyasirid, lucinid, vesicomyid and solemyid bivalves (Holmes et al. 2005; Oliver & Sellanes 2005; Sellanes & Krylova 2005) as well as siboglinid tubeworms (i.e. vestimentiferan and frenulata). Previous studies in this area indicate that the photosynthesis-derived carbon is the main pathway of incorporation of carbon in the heterotrophic megafauna collected by trawl (Sellanes et al. 2008). However, these samples included only megafauna and were obtained from the edge of a much larger seep province, as recently estimated by Klaucke et al. (2012). The ecological role of the smaller-sized fauna in the food web at the CMSA is mostly unknown, as is the overall role of the whole assemblage in methane cycling and benthic carbon flux. The Chilean margin represents one of the largest reservoirs of methane on the planet (Morales 2003), thus identifying how the infaunal food web uses methane is important for a larger understanding of methane seep processes and global biogeochemical cycles.

Here we report on the CMSA community and its trophic structure based on the first directed infaunal community collected with visual guidance in association with a multiple-corer (TV-MUC), grab (TV-Grab), and a remotely operated vehicle (ROV), in combination with megafaunal taxa collected by trawl. These samples from active seep sediments allow us to determine the relative proportion and type of chemosynthetic energy that fuels this chemosynthetic community, including the relative input of methane-derived carbon. The objectives of this study are thus: (i) to assess the origin of the carbon source incorporated by heterotrophic seep fauna in the CMSA, (ii) to quantify the amount of methane-derived carbon incorporated into the fauna, identifying the species that may specialize upon feeding of methanotrophic microbes, and (iii) to evaluate the trophic positions for members of this methane seep community and the isotopic niche width in predatory fishes.

Material and Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Appendix 1: Carbon and nitrogen isotopes ratios of heterotrophic macro and megafauna in the CMSA. Trophic positions are estimated by nitrogen isotope ratios and feeding modes according to indicated references

Site characteristics and sample collection

The Concepción methane seep area (CMSA) is located ~72 km NW off the Bay of Concepción (36°22′ S; 73°73′ W) at the mid-slope (~700 m water depth) (Fig. 1). The sediment surface is characterized by the presence of abundant carbonate-cemented mud blocks (Sellanes et al. 2004, 2008; Quiroga & Sellanes 2009), while high concentrations of reduced compounds, including over 30 mm methane and 10 mm sulfide, as well as gas hydrates, have been documented in sediment cores (Coffin et al. 2006). Recent studies indicate that the CMSA is just a portion of one of the largest cold seep areas known at active continental margins (Klaucke et al. 2012) extending from ~ 35°50′ S to 36°34′ S and including both active and fossil seep sites.

image

Figure 1. Map of the study area including different sampling stations in the Concepción Methane Seep Area (CMSA) (Ocean Data View map; Schlitzer 2012). Cruises: VG07 (Vidal Gormaz-2007), INSPIRE (International South-East Pacific Investigation of Reducing Environments), ChiFlux (Sonne-210). Numbers indicate the correlative number assigned to each station on the map and are summarized in Table 1. The solid line box indicates the approximate extension of the CMSA, as reported by Klaucke et al. (2012).

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Samples were collected during three cruises: VG07 (September 2007, R/V Vidal Gormáz), INSPIRE (February–March 2010, R/V Melville) and ChiFlux (September–November 2010, R/V Sonne) (Table 1). Macro- and megafauna samples were obtained with an Agassiz-type trawl (AGT; horizontal opening of 1.5 × 0.5 m and a mesh of 10 × 10 mm), multi-core (MUC), video-guided multi-corer (TV-MUC), video-guided grab (TV-Grab) and the remotely operated vehicle ROV Kiel 6000 (see http://www.geomar.de/en/institute/central-facilities/technology-logistics-centre/rovkiel6000) (Table 1). The ROV sampled carbonate fragments via the robotic arm and megafauna using scoop nets. The TV-Grab had a penetration depth of 0.5–1 m (a sample volume of around 1 m3).

Table 1. Sampling sites, dates, depth, habitat and gear used for samples collection. ‘Mixed’ are areas where more than one type of habitat can occur sampled via epibenthic trawl. Station code corresponding to numbers assigned to each station on the map (see Fig. 1)
CruiseStationDate (dd/mm/yr)GearLatitude (S)Longitude (W)DepthHabitatStation code
VG07AGT1002-10-2007AGT36°22.000′73°43.003′764Mixed1
AGT1103-10-2007AGT36°21.024′73°42.028′824–730Mixed2
AGT1304-10-2007AGT36°21.022′73°43.011′855Mixed3
AGT1404-10-2007AGT36°21.026′73°43.004′842Mixed4
INSPIRE2808-03-2010TV-MUC36°22.200′73°42.992′817Clam/Mat5
2908-03-2010TV-MUC36°22.199′73°42.993′797Clam/Mat6
3209-03-2010TV-MUC36°22.235′73°42.993′813Clam/Mat7
4210-03-2010AGT36°22.523′73°43.115′724–764Mixed8
4410-03-2010AGT36°24.010′73°43.074′769–766Mixed9
4510-03-2010AGT36°22.999′73°43.997′766–906Mixed10
4611-03-2010AGT36°22.425′73°43.073′753–761Mixed11
4711-03-2010AGT36°21.937′73°43.099′840–816Mixed12
ChiFlux1602-10-2010TV-MUC36°28.217′73°40.729′699Black sediment13
2504-10-2010ROV36°21.997′73°42.785′775Clam/Mat14
5413-10-2010TV-MUC36°28.222′73°40.724′707Clam/Mat15
6415-10-2010TV-GRAV35°58.558′73°38.427′1034Carbonate16
6916-10-2010TV-GRAV36°24.950′73°42.150′680Carbonate17
7417-10-2010ROV36°26.489′73°41.359′706Clam/Mat18
7818-10-2010ROV36°25.234′73°42.169′664Tubeworm/Clams19
8419-10-2010ROV36°22.870′73°42.687′687Carbonate20
8820-10-2010ROV36°22.960′73°42.135′700Pogonophoran field21
9121-10-2010TV-MUC36°28.140′73°40.749′706Clam/Mat22
9522-10-2010ROV36°23.759′73°42.267′698Carbonate23
9823-10-2010ROV35°59.749′73°38.389′927Tubeworm/Clams/Mat24

Samples for bottom-water particulate organic matter (POM) were collected during the VG07 cruise, using a Rosette with 12 × 8-l Niskin bottles. Approximately 2 l of water were pre-sieved through a 63- μm mesh to remove large-sized zooplankton and large detrital particles, and then filtered through pre-combusted (500 °C for 4 h) Whatman GF/F filters (0.7 mm nominal pore size). Because in this study there were no replicates for POM signatures, data reported by Sellanes et al. (2008) were pooled to estimate the average POM values of the area. The sedimentary organic matter (SOM) value reported by these authors was also included to obtain a reference signature for this area (Fig. 2).

image

Figure 2. Biplot of δ13C and δ15N values of all the heterotrophic fauna, symbiont-bearing fauna and potential food sources collected in the CMSA. Isotopic signatures of dominant pelagic species are also included as references values. SOM, sedimentary organic matter; POM, particulate organic matter. Vertical and horizontal error bars represent the standard deviation (SD).

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Sample preparation

A total of 301 samples were processed live after identification to the lowest possible taxon, including in most cases only one individual per species (Appendix 1). For large fauna, appropriately 0.7 mg of tissue was dissected, washed with Milli-Q water, placed in pre-combusted vials and frozen at −80 °C for later analysis. Infauna samples were allowed to evacuate their guts overnight into 25-μm filtered seawater (FSW) and then frozen whole after being rinsed in Milli-Q water. Upon return to the laboratory, samples were dried in an oven (60 °C) for 12 h. Due to the high lipid content in the tissues of some fishes, lipids were removed by agitating the tissue in chloroform: methanol (1:1) solution for 30 min (Folch et al. 1957; Bligh & Dyer 1959). This procedure was repeated at least three times, until a clear solution was obtained. Again, the tissues were rinsed with Milli-Q water and dried in an oven (40 °C) for 12 h. When appropriate, tissue samples were ground into a fine powder with an agate mortar; the tissue samples were then acidified with 1% PtCl2 in a 1 n HCl solution to remove inorganic carbonate. Finally small amounts of tissue (~ 0.5 mg) were placed in pre-weighed tin capsules and stored in a desiccator until stable isotope analysis.

Stable isotopes analysis

The isotope composition was analysed in the School of Biological Sciences, Washington State University, on a Eurovector elemental analyzer coupled to a Micromass Isoprime isotope ratio mass spectrometer. Stable isotope ratios are reported in the δ notation as the deviation from standards (Vienna Pee Dee Belemnite for δ13C and atmospheric N2 for δ15N), so δ13C or δ15N = [(R sample/R standard) − 1] × 103, where R is 13C/12C or 15N/14N, respectively. Typical precision of the analyses was ± 0.5‰ for δ15N and ± 0.2‰ for δ13C.

Contribution of MDC in heterotrophic fauna

Estimates of the percentage of methane-derived carbon (Fm) in the macro- and megafauna of the CMSA were generated using a two-source, single isotope mixing model as in Fry & Sherr (1984). Fm was given by the formula:

  • display math

where δF, δm and δPOM are the carbon isotopic signatures of fauna, methane and particulate organic matter of bottom water (POM), respectively. Fm was calculated using the δ13C values for each macro- and megafauna individual sampled and then the mean was taken to generate values for each taxa. The δPOM was measured as the average value of POM published by Sellanes et al. (2008) and those measured in this study (mean δ13C = −24.0‰, Table 2). This method may overestimate the amount of methane used by individuals that consume sulfide-oxidizing bacteria and to correct for this we have replaced δPOM with δSOB, where δSOB is the average δ13C value of fauna bearing sulfide-oxidizing bacteria (SOB) estimated for the area (δ13C = −32.6‰). This provides a conservative, albeit wide-ranging, estimate of MDC. The δ13C of methane may vary both spatially and temporally (Ziebis & Haese 2005), therefore, extreme values of methane were used: δm values = −63.1 and −61.4‰ as reported for the CMSA by Pohlman et al. (2009). No trophic shift between animal tissue and carbon source was taken into account, as this is considered negligible (< 1‰; Vander Zanden & Rasmussen 2001; McCutchan et al. 2003).

Table 2. δ13C and δ15N values of potential food sources and symbiont-bearing species in the CMSA
Potential food sourcesδ13Cδ15NnSC
MeanSDMeanSD
  1. a

    Value obtained from Sellanes et al. (2008).

  2. b

    Values pooled with data reported by Sellanes et al. (2008).

  3. SD = standard deviation; n = number of samples analysed; SOM = sedimentary organic matter; POM = particulate organic matter; SC = station code on the map (Fig. 1).

Photosynthetic origin
SOM−20.28.81 a
POM−24.01.09.01.63 b
Chemosynthetic origin
Filamentous Bacteria−24.216
Frenulata sp.−32.14.317
Lamellibrachia sp.−30.2, −27.05.2, 5.3219
Thyasira methanophila−34.00.18.21.431, 13, 15
Calyptogena gallardoi−34.60.43.53.551, 13, 14
Archivesica sp.−33.37.7124

Trophic position of heterotrophic fauna

The calculation of the consumer trophic position was performed using the equation detailed by Vander Zanden & Rasmussen (1999), which has been widely used in marine ecosystems (e.g. Iken et al. 2001, 2010). Trophic position was calculated using the equation:

  • display math

where TPconsumer is the estimation of the trophic position of the consumer, δ15Nconsumer is the measured δ15N value in the consumer analyzed. Due to the high isotopic variability of potential primary consumers (e.g. suspensivores and depositivores), the value of the sedimentary organic matter (SOM) was used as the base signature (δ15NSOM), assuming that this is the main nutritional source for primary consumers at the base of the food web. The constant 1 corresponds to the level of primary sources to the food web (Iken et al. 2010). A value of 3.4‰ is usually assumed as the average enrichment in δ15N per trophic level (Minagawa & Wada 1984; Post 2002).

Isotopic niche width in demersal predator fishes

Additionally, the Bayesian standard ellipse areas (SEAB) were estimated to compare the isotopic niches of two benthic predators, the Patagonian toothfish Dissostichus eleginoides and the combtooth dogfish Centroscyllium nigrum, based on the data points of all individuals in the δ13C and δ15N bi-plot space (Jackson et al. 2011). This value or area represents a measure of the total amount of niche space occupied by the population, and is a proxy for the total extent of trophic diversity and utilized resources. It is analogous to the total area of the convex hull (TA) originally proposed by Layman et al. (2007) but uses Bayesian multivariate ellipses. Bayesian inference techniques, propagating sampling error on the estimates of the means, allow robust statistical comparisons between datasets with different sample sizes (Jackson et al. 2011). SEAB measurements were calculated using the routine SIBER (Stable Isotope Bayesian Ellipses in R– Jackson et al. 2011) incorporated in the SIAR package. Statistical analyses and SIAR calculations were performed using r 2.12.2 software (R Development Core Team 2011).

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Appendix 1: Carbon and nitrogen isotopes ratios of heterotrophic macro and megafauna in the CMSA. Trophic positions are estimated by nitrogen isotope ratios and feeding modes according to indicated references

Symbiont-bearing fauna and bacteria

We collected five species of symbiont-bearing fauna. Their isotopic signatures reflected symbionts with similar carbon fixation pathways – sulfide oxidation (Table 2). Bivalves belonging to the family Vesicomyidae (Archivesica sp. and Calyptogena gallardoi) and Thyasiridae (Thyasira methanophila), and polychaetes of the family Siboglinidae (Frenulata and Lamellibrachia sp.) had a total δ13C range of 6.0‰ around the mean for each of the species. Calyptogena gallardoi had the most 13C-depleted average isotopic values (δ13C = −34.6 ± 0.4‰, n = 5) and Lamellibrachia sp. the least depleted values (δ13C = −28.6 ± 2.2‰, n = 2). Co-occurring filamentous bacteria, likely belonging to the Beggiatoa or Thioploca genera, were less 13C-depleted (δ13C = −24.2‰, n = 1) than the symbiont-bearing metazoa, but only a single sample was analyzed from this taxon. The chemosymbiotic fauna had a total range of δ15N of 4.6‰. C. gallardoi again had the least 15N-enriched values (δ15N = 3.5 ± 3.5‰, n = 5) and T. methanophila the most 15N-enriched values (δ15N = 8.2 ± 1.4‰, n = 2).

Diet of heterotrophic fauna

A total of 97 presumably heterotrophic macrofaunal taxa and 86 megafauna were analysed (totaling 273 samples; Fig. 2, Appendix 1). The assemblage exhibited a very broad range of δ13C values (span of 42.9‰). A sipunculid (sp. 8; Table 3) had the most 13C-depleted value (δ13C = −48.1‰, n = 1), and a chiton species (Polyplacophora) the least 13C-depleted value (δ13C = −5.2‰, n = 1). Moreover, the δ15N values equally had a wide variation, with a range of 32.2‰. The foraminiferan Globobulimina sp. had the most 15N-depleted value (δ15N = −9.6‰) and the predatory chiton Placiphorella sp. the most 15N-enriched value (δ15N = 22.6‰; Appendix 1). The taxa Cumacea sp. 1, Nematoda sp. 2, Tanaidacea sp. 2, Neolepetopsidae sp., Pyropelta sp. and Nemertea sp. 2 also had 15N-depleted values (≤ 6.0‰; Table 3 and Appendix 1), which were similar to those reported for symbiont-bearing fauna (mean δ15N = 5.4‰) and lower than δ15N of the particulate organic matter (POM, mean δ15N = 9.0‰) and sedimentary organic matter (SOM, δ15N = 8.8‰; Table 2).

Table 3. δ13C and δ15N (mean and standard deviation) composition and contribution (Fm min and Fm max) of methane-derived carbon (MDC) in heterotrophic taxa tissues
PhylumSpecies513CSDδ15NSDn Fm minFm maxTPSDFeeding modeReferencesSC
  1. TP = trophic position; n = samples number; SF = suspension-feeder; DF = deposit-feeder; C = carnivore; G = grazer; ? = indeterminate feeding mode; SC = station code on the map (see Fig. 1 and Table 1).

PoriferaSuberites puncturatus−27.118.2108.33.8SFRibes et al. (1999)17
Demospongidae sp. 2−30.110.61016.31.5SFRibes et al. (1999)17
NematodaNematoda sp. 2−24.84.44.34.5302.0−0.31.3?6, 8, 10
SipunculaSipunculidae sp. 8−48.17.7139.864.40.7DFMurina (1984)16
Sipunculidae sp. 7−26.114.3105.62.6DFMurina (1984)16
Anne lidaCirratulidae sp. 2−26.06.6105.30.4DFFauchald & Jumars (1979)1
Cossuridae sp. 1−26.6107.0DFRomero et al. (2004)6
Nereis sp.−31.29.61019.31.2CFauchald & Jumars (1979)18
Nereididae sp. 1−40.19.11 19.443.11.1CFauchald & Jumars (1979)4
Polychaeta sp. 2−30.68.41017.50.9? 
Polynoidae sp. 1−24.34.914.52.6300.63.20.3CFauchald & Jumars (1979)1
Terebellidae sp. 2−25.59.2103.91.1DFFauchald & Jumars (1979)22
MolluscaMargarites huloti−31.6, −18.411.2, 17.7202.62.7GSmith et al. (1985)17, 23
Neolepetopsidae sp.−43.85.3128.752.90.0GSasaki et al. (2010)16
Provanna sp.−33.0, −37.37.5, 6.026.729.80.4GLevin & Michener (2002)14
Pyropelta sp.−43.56.0128.052.10.2GSmith & Baco (2003)14
ArthropodaAmphipoda sp. 1−24.610.6101.51.5SFThiel et al. (2003)4
Amphipoda sp. 3−33.87.213.126.10.5SFThiel et al. (2003)16
Caprella sp.−25.610.1104.31.4SFThiel et al. (2003)2
Cumacea sp. 2−30.4 4.51017.1−0.3DFThiel et al. (2003)9
Echinode rmataSterechinus cf. neumayeri−27.413.0109.02.2GNorkko et al. (2007)17
Lophaster stellans−31.37.2 1019.50.5CAnderson & Shimek (1993)16

MDC in heterotrophic fauna

A total of 22 taxa (including 28 samples) recorded Fm values > 1% at the upper limit (Fm max) for MDC (Table 3). These included species with different feeding modes (i.e. deposit-feeding, suspension-feeding, grazers, carnivores and indeterminate feeding mode) belonging to a diversity of taxa (e.g. sipunculids, polychaetes, gastropods, peracarids and echinoderms; Table 3). The maximum estimate of MDC was observed in Sipunculidae sp. 8 (Fm = 39.8–64.4%), followed by gastropods (Neolepetopsidae sp., Fm = 28.7–52.9% and Pyropelta sp., Fm = 28.0–52.1%) and a Nereididae sp. 1 (Fm = 19.4–43.1%). The gastropod Provanna sp. and the peracarid Amphipoda sp. 3 exhibited intermediate MDC values (Fm = 6.7–29.8% and 3.1–26.1%, respectively; Table 3).

Trophic structure of consumers

A broad range of trophic niches was observed among analyzed consumers (δ15N range), and three trophic levels of consumers were estimated. The first-order consumers (species that feed directly on primary sources) included a total of 57 taxa belonging to eight phyla; the majority of these taxa were from the Annelida, Arthropoda, Sipunculida and Mollusca. The annelids were represented mainly by polychaetes, including some families known as carnivorous (e.g. glycerids, polynoids, syllids) and deposit-feeders (e.g. ampharetids, capitellids, cirratulids). The arthropods were represented by peracarid, cirriped, ostracod and decapod crustaceans. The molluscs included mainly gastropods, a scaphopod and bivalves. Unexpectedly, among fishes only the blue hake Antimora rostrata was positioned in this basal trophic level (TP = 2.7 ± 0.1; Fig. 3).

image

Figure 3. Trophic position (TP) of benthic predatory fishes from the methane seep area. Standard deviations (SD) of the TP are also included. Circles represent osteichthyes fishes and triangle chondrichthyes fishes.

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The second-order consumers (carnivores and omnivores which preferentiality feed on the primary consumers) included the largest number of species (i.e. 66 taxa). Deposit-feeders and suspension-feeders were present in the polychaetes that occupy this trophic level. Further, among molluscs the gastropod Iothia megalodon had a high trophic position (TP = 3.9) suggesting a heterotrophic feeding mode (carnivore or omnivore diet). Two osteichthyes fishes (Myctophidae sp. 2 and Hygophum sp.) and the combtooth dogfish Centroscyllium nigrum also were found to generally belong to this trophic level.

The third-order consumers (carnivores and omnivores which preferentiality feed on the secondary consumers) were composed of 27 taxa, including macrourid osteichthyes fishes. In this trophic level the macrourid fishes (i.e. unidentifiable Macrouridae sp., Macrourus holotrachys and Coryphaenoides ariommus) occupied the highest trophic positions (TP = 4.6) (Fig. 3). However, the Patagonian toothfish Dissostichus eleginoides and the Dusky cat shark Bythaelurus canescens had a wide variation in the δ15N values and may thus exhibit a variety of trophic positions including that of top predators (TP = 4.1 ± 0.8 and 4.4 ± 1.2, respectively; Fig. 3). Alternatively, they may consume diet items that vary broadly in δ15N signatures, possibly reflecting DIC variations.

Finally, the polyplacophoran Placiphorella sp. registered the highest trophic position (TP = 5.1), as indicated by the high 15N-enrichment in their tissues. Moreover, it is important to note that an anomalous trophic position was observed in several animals (e.g. protozoan, polychaetes, cnidarians; TP = ≤2.0; Appendix 1) due to 15N-depleted values in their tissues (δ15N ≤ 7.7‰), which in most cases were associated with the consumption of chemosynthetic sources (registered MDC contribution, Table 3) or from additional microbial food sources that remain uncharacterized in this analysis (highly 15N-depleted).

Isotopic niche width of fishes

The Bayesian standard ellipse areas (SEAB) estimated for D. eleginoides and C. nigrum indicate differences in the isotopic niche width (Fig. 4), with an average value of 12.4‰2 (7–23‰2, 95% Bayesian confidence interval) and 4.5‰2 (2.6–7.7‰2, 95% Bayesian confidence interval), respectively.

image

Figure 4. Convex hull encompassing all the data points (dashed line) and Bayesian standard ellipses area (SEAB; black ellipses) in the δ13C-δ15N bi-plot space for two benthic predatory fishes in the CMSA, the Patagonian toothfish Dissostichus eleginoides (black circles) and the combtooth dogfish Centroscyllium nigrum (open circles).

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Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Appendix 1: Carbon and nitrogen isotopes ratios of heterotrophic macro and megafauna in the CMSA. Trophic positions are estimated by nitrogen isotope ratios and feeding modes according to indicated references

Isotopic composition of chemosymbiotic fauna

The overall carbon isotopic composition of known symbiont-bearing fauna from the CMSA (δ13C range = −34.6 to −28.6‰) indicates that the main energy source for these taxa was derived from thiotrophic symbionts (i.e. sulfide-oxidizing bacteria; Cavanaugh et al. 2006). Thyasirid bivalves are known to harbor endosymbiotic bacteria in their gills (Dando et al. 2004) and also to have the capacity for heterotrophic feeding (Dando & Spiro 1993). In this study, the isotopic value of T. methanophila, δ13C = −34.0‰ is clearly divergent from photosynthetic values, indicating that this species relies on chemoautotrophic food sources, a similar result found based on scanning electron microscopy by Oliver & Sellanes (2005). Lamellibrachia sp. was less 13C-depleted (δ13C = −28.6‰ ± 2.2) than other symbiont-bearing fauna from the CMSA, but more 13C-depleted than previously reported for this site and species (δ13C = −22.8‰; Sellanes et al. 2008). The δ13C values of vestimentiferans are influenced by dissolved inorganic carbon (DIC) sources and their proportions, growth rate, and morphology of individuals (Fisher et al. 1997; MacAvoy et al. 2005). Vestimentiferans potentially take up DIC from both the sediment across their roots as well as from the water column through their plumes, each with its own carbon isotopic signature, leading to different tissue δ13C values even if the same energy source was used (MacAvoy et al. 2005 and references therein). There is also a great deal of spatial variation in DIC leading to broad ranges in δ13C values among Lamellibrachia individuals in New Zealand seeps (Thurber et al. 2010). At the CMSA, frenulate siboglinids (pogonophorans) also had an isotopic composition typical of reliance on thiotrophic bacterial symbionts (δ13C = −32.1‰, δ15N = 4.3‰; Levin 2005). Similar carbon isotope values have been found in frenulates living at methane seeps in the Gulf of Alaska (δ13C = −38‰ and δ15N = 2.4‰; Levin & Michener 2002), Sea of Okhotsk (δ13C range = −38.0 to −30.5‰; Sahling et al. 2003), Hikurangi Margin off New Zealand (e.g. −38.6 to −33.5‰; Thurber et al. 2010), which are slightly more enriched than values of Oligobrachia haakonmosbiensis obtained from Haakon Mosby Mud Volcano (−66.7‰, Lösekann et al. 2008). These were the first collections of frenulates from this region, although recent surveys have found extended fields of this potentially novel species. It is interesting that they have similar isotopic values to those individuals collected on the other side of the Pacific Ocean, suggesting similar roles in the benthic ecosystems. A series of video and images captured by the ROV Kiel 6000 (GEOMAR) suggests that this species is potentially consumed by the shrimp Haliporoides diomedeae or that the shrimp feed on organic matter trapped in the tubes (Fig. 5A).

image

Figure 5. Sea-floor images of fauna living in the CMSA taken with the Ocean Floor Observation System (OFOS; see Treude et al. 2011) and ROV Kiel 6000 during ChiFlux cruise. (A) Unidentified frenulate field and shrimp (Haliporoides diomedeae) feeding on them (ROV#9, SC = 21). (B) Gastropod Neolepetopsidae sp. probably grazing on epibiotic bacteria of the vesicomyid Archivesica sp. (ROV#11, SC = 24). (C) Unidentified asteroid in the vicinity of Lamellibrachia sp. aggregations (ROV#7, SC = 19). (D) Echinoids Sterechinus cf. neumayeri grazing on the tubeworms Lamellibrachia sp. (OFOS#1). (E) Echinoid Dermechinus horridus apparently grazing on bacterial mats (arrows) (ROV#11, SC = 24). (F) Macrurids and hagfish swimming over a clam field (ROV#2, SC = 14). Scale bars: 2.5 cm (A,B), 10 cm (C,D), 3 cm (D) and 10 cm (E). SC, Station code on the map and Table 1.

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Incorporation of chemosynthetic production by heterotrophic fauna

The wide variation of δ13C (42.9‰) in the heterotrophic fauna, indicate that a diversity of carbon sources fuel this habitat. These carbon sources come from a variety of types of chemoautotrophic production (e.g. methanotrophy and thiotrophy) and photosynthetic production and supporting a high trophic diversity among consumers. Greater than 87.5% of the species studied registered δ13C values > −24‰, indicative of incorporation of photosynthesis-derived organic matter. The remaining 12% registered highly negative δ13C values (<−24‰), indicating some chemosynthetic carbon incorporation (e.g. methanotrophy ≤−40‰ and thiotrophy = −35.2 to −24.3‰; MacAvoy et al. 2002; and references therein; Table 2).

Gastropods at seeps and vent habitats have been shown to host symbionts, deposit-feed and prey upon other invertebrates. One relationship that has been enigmatic to understand is the relationship between neolepetopsid limpets and the variety of hosts that they live upon. Members of this family typically live on bivalves and vestimentiferan tubes (Sasaki et al. 2010), and the neolepetopsid limpets found at the CMSA occurred growing on the chemosymbiotic bivalve Archivesica sp. (Fig. 5B). In this study the δ13C and δ15N values of the neolepetopsids were even more 13C-depleted than the tissues of the clam Archivesica sp. (Table 2) and Fm values of these limpets suggest a considerable methane-derived carbon incorporation (Fm min, max = 28.7–52.9%), as would be expected if it grazed on a diverse food source including both free-living thiotrophic and methanotrophic bacteria or archaea (Cordes et al. 2010b). Some species belonging to this family, feed on small invertebrates (Warén & Bouchet 2001, 2009; Warén et al. 2006), yet this was unlikely, as the neolepetopsids had an isotopic composition indicative of a primary consumer. Neolepetopsids may graze on authigenic carbonates, feeding directly on microbes precipitating the rocks, which often have low δ13C values (Levin et al. unpublished). Aerobic methanotrophy could offer an alternative food source, similar to that observed in hydrothermal ecosystems off Costa Rica (Levin et al. 2012); although this metabolic pathway has yet to be characterized at the CMSA, free-living aerobic methanotrophs may be abundant in surface sediments (Lösekann et al. 2007).

Gastropods of the genus Provanna are among the most often observed taxa in vents and seeps (Warén & Bouchet 2001), and are considered deposit-feeders (Warén & Bouchet 1986; Warén & Pounder 1991). However, Provanna sp. from the CMSA had 13C-depleted values (δ13C = −35.2 ± 3.1‰) that were similar to those of symbiont-bearing fauna. Similar negative values have been reported for vent and seep congeners: Provanna sp. (Levin & Michener 2002), Provanna lomana (Smith & Baco 2003), Provanna sculpta (MacAvoy et al. 2005; Cordes et al. 2010b), Provanna variabilis (Bergquist et al. 2007), Provanna sp. (Olu et al. 2009), and Provanna laevis (Soto 2009), in all cases suggesting grazing on free-living bacteria (e.g. among mytilid beds, vestimentiferan tube-worms, and upon bacterial mats) or nutrition from endosymbionts (Smith & Baco 2003; MacAvoy et al. 2005; Bergquist et al. 2007). Nevertheless, this latter case is unlikely since the ctenidium of Provanna is not hypertrophied, unlike in Alvinoconcha and Ifremeria (Sasaki et al. 2010).

The amount of seep production incorporated by mobile predators (e.g. echinoderms, decapods, fishes) can be an indicator of the residence time of these species in the methane seeps (Carney 2010). At the CMSA, the asteroid Lophaster stellans and the echinoid Sterechinus cf. neumayeri clearly assimilated chemosynthetically derived carbon via sulfide oxidation (Table 3). Both species had isotopic values that reflected a mixture of seep and photosynthetic production. Predation on symbiont-bearing fauna (e.g. vestimentiferan polychaetes) could possibly occur in some asteroids of this area (Fig. 5C). However, in the case of Sterechinus cf. neumayeri they could be grazing on the Lamellibrachia sp. tubes (Fig. 5D) since these tubes often harbor free-living chemoautotrophic bacteria (Julian et al. 1999) that may be an important food source for this echinoderm taxa. Another option could be the consumption of bacterial filaments, as suggested by in situ images of the echinoid Dermechinus horridus within the area (Fig. 5E).

Trophic structure of benthic consumers

Although diverse macro- and megafauna are the primary consumers at the CMSA, a variety of species occupied higher trophic levels (Appendix 1). The use of δ15N to identify the trophic level has the underlying assumption that there is a constant δ15N at the base of the food web. This assumption at methane seeps is often not valid as a variety of sources, including some of the symbiont-bearing taxa identified here, had 15N-depleted values (e.g. Calyptogena gallardoi, δ15N = 3.5‰). These species could provide a potential food source for grazers and scavengers, therefore affecting their isotopic composition and lead to a consumer being assigned to a lower trophic level. An alternative explanation could be that the high percentage of microbial production, as well as the large physical size of certain bacteria in bathyal habitats (i.e. Gallardo 1977) leads to an expansion of the trophic niche in traditional carnivores to an omnivorous diet, where consumers can feed on both chemoautotrophic producers (e.g. bacteria that fix local nitrogen) and small invertebrates (Fanelli et al. 2009; Hoyoux et al. 2009). Further, it is worth noting that both deposit-feeding and suspension-feeding taxa had wide ranges of δ13C and δ15N, which could be associated with temporal and spatial variability in the quality and quantity of food (Iken et al. 2001) or the exploitation of organic matter in different stages of degradation (e.g. fresh detritus to highly refractory; Grémare et al. 1997). Moreover, anomalously low nitrogen isotopic composition likely indicates the incorporation of seep production, as seep microbes may use local nitrogen sources that result in low δ15N values (Levin & Mendoza 2007) or the fauna themselves may assimilate DIN or DON from the available N pool. On the other hand, bivalve species can consume particulate organic matter (POM) and also feed on dissolved organic matter; this last nutritional alternative also has been suggested for deposit-feeding species (Lopez & Levinton 1987) and numerous invertebrate phyla (e.g. Porifera, Annelida, Mollusca, Sipunculida; Sepers 1977). Therefore, the base of the food web at seeps is complex, where numerous food sources may be exploited by consumers and yet these are masked by shifting nitrogen isotopic values and divergent nitrogen isotopic ratios at the base of the food web.

Although applying isotopic trophic approaches to seep systems entails many challenges and assumptions, in most instances the results are consistent with the known natural history of the taxa considered in the analysis. Deep-sea chitons typically feed on sponges, hydroids and corals (Gracia et al. 2005); this agrees with the trophic positions estimated for all polyplacophoran taxa analysed in this study (i.e. Leptochiton sp., Leptochiton americanus, Stenosemus sp., and Polyplacophora sp.) (TP = 3.8 to 5.1; Appendix 1). The high trophic position of the polyplacophoran Placiphorella sp. in this area (TP = 5.1) may be associated with a peculiar morphological adaptation that it possesses to trap prey; this genus has an enlarged anterior girdle that is employed to trap mobile food sources, including other animals (McLean 1962; Eernisse et al. 2007).

The Patagonian toothfish Dissostichus eleginoides and the dusky cat shark Bythaelurus canescens were the top predators of the methane seep food web at the CMSA (Fig. 3). Both species are vagrants at methane seeps (sensu Carney 1994) and are likely attracted by the diversity of prey available in these environments (Sellanes et al. 2008). Indeed, D. eleginoides was significantly more abundant at the CMSA than at the surrounding area (Sellanes et al. 2012). Moreover, D. eleginoides was identified as a generalist consumer and omnivore based on its wider isotopic trophic niche (indicated by its larger SEAB area). This agrees well with observations of Flores & Rojas (1987), who concluded that this species is a non-selective carnivore that consumes a diversity of prey species (Garcia de la Rosa et al. 1997) with a seasonally variable diet (Murillo et al. 2008). In contrast, a more specialized feeding behavior was detected in the combtooth dogfish Centroscyllium nigrum, based on the estimation of the SEAB area. The trophic position estimated for C. nigrum (TP = 3.9; Fig. 2) agrees with the known trophic position of its congener Centroscyllium fabricii, TP = 3.8 (Cortés 1999). The blue hake Antimora rostrata occupied a lower trophic level (Appendix 1), probably reflecting a diet based on pelagic/benthopelagic and benthic prey, as has been observed in individuals inhabiting the Atlantic Ocean (Houston & Haedrich 1986). The consumption of carrion has been widely observed in this species (Collins et al. 1999; Yau et al. 2002; Kemp et al. 2006) and abyssal macrourids (Drazen et al. 2008; Jeffreys et al. 2010) linking benthic and pelagic trophic pathways (Iken et al. 2001). On the other hand, despite the absence of isotope values that reflect incorporation of chemosynthetic production in the fish species, the presence of numerous macrourids and hagfishes on the chemoautotrophic assemblages (i.e. clam field) suggests a potential ecological relationship between these faunal groups (e.g. trophic, refuge, nursery; Fig. 5E) as reported by Treude et al. (2011).

Food web length (FWL) is a measure of trophic links from primary producers to top predators in an ecosystem, and has been considered a key aspect of food webs, since it regulates a wide range of ecological processes (Kondoh & Ninomiya 2009), plays a role in regulating biogeochemical fluxes, and influences fisheries productivity (Vander Zanden & Fetzer 2007 and references therein). Although examples of FWL in benthic deep-sea environments are scarce, three trophic levels have been estimated in the Algerian Basin (650–780 m; Fanelli et al. 2009), Porcupine Abyssal Plain (~4840 m; Iken et al. 2001), and Håkon Mosby Mud Volcano (~1250 m; Gebruk et al. 2003), agreeing with the average FWL estimated for other marine ecosystems (3.97 ± 0.47; Vander Zanden & Fetzer 2007). However, for the bathyal food web at the CMSA, four trophic levels were estimated, as in the Arctic Canada Basin (625–3900 m; Iken et al. 2005) and the Blake Ridge methane seep (~2155 m; Van Dover et al. 2003). At present, it is recognized that heterogeneity generated by carbonate reefs and a number of associated bioengineer species (e.g. tubeworms, corals, sponges, bivalves, Levin & Dayton 2009; Cordes et al. 2010a; Govenar 2010), increase the richness and diversity in these environments, attracting a large number of non-seep taxa of different trophic levels (e.g. echinoderms, fishes, gastropods, shrimps). These taxa exploit chemosynthetic production and increased habitat diversity for the benefit of their feeding, in turn generating more complex trophic interactions at these sites over time.

Conclusions

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Appendix 1: Carbon and nitrogen isotopes ratios of heterotrophic macro and megafauna in the CMSA. Trophic positions are estimated by nitrogen isotope ratios and feeding modes according to indicated references

The CMSA is composed of numerous microhabitats which are spread over an extensive area that so far has been rarely studied in terms of fauna and ecological processes. Therefore, numerous new species and novel ecological aspects are expected to be discovered in the coming years. This study reveals a series of trophic attributes of consumers inhabiting the CMSA which in part help to identify the trophic ecology of reducing communities, the roles of consumers in the deep-sea food web and the heterogeneous carbon sources utilized by chemosymbiotic and heterotrophic fauna. The finding that much of the heterotrophic fauna at CMSA does not depend solely on seep production emphasizes the strong integration of chemosynthetic and photosynthetic processes on margins, and the potential sensitivity of seep habitats to climate change and other external influences on surface production. This work also helps us to understand the long-term biogeochemistry of seep system and the ecology of the species that are associated with it, including those that are not obligate seep species. The trophic connections identified here provide the foundation for an ecosystem model that can be used in the conservation of these environments and their resources. Such models increase in importance as human exploitation of fishes, energy and minerals expands in both methane seep and non-seep deep-sea environments of the Southeastern Pacific.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Appendix 1: Carbon and nitrogen isotopes ratios of heterotrophic macro and megafauna in the CMSA. Trophic positions are estimated by nitrogen isotope ratios and feeding modes according to indicated references

We thank the captain, crew and scientific party of R/V Vidal Gormáz (VG-07 cruise), R/V Melville (INSPIRE cruise) and R/V Sonne (ChiFlux cruise) for support at sea. We especially thank Francisco Valdés (UCN) for collecting samples during the ChiFlux cruise. We thank Bernhard Bannert and the whole ROV Kiel 6000 team for technical support during the OFOS, TV-MUC, TV-grab and ROV deployments on R/V Sonne. Financial support for the ChiFlux cruise came through the Collaborative Research Center (SFB) 574 (‘Volatiles and Fluids in Subduction Zones’) funded by the DFG, contribution No. 255. Ship time for INSPIRE was funded by the University of California Ship Funds, Scripps Institution of Oceanography, and participation of GZ-H and other Chilean researchers in the cruise was funded in part by a grant of the program COMARGE and ChEss of the Census of Marine Life. Additional support to G.Z.-H. during the writing of this manuscript was provided by the Center of Oceanographic Research in the Eastern South Pacific (COPAS) of the University of Concepción, and L.A.L. was supported in part by NSF OCE 0826254. This work was funded by FONDECYT project No. 1100166 to J.S., and partial support during the writing phase was provided by FONDECYT project No. 1120469.

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  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Appendix 1: Carbon and nitrogen isotopes ratios of heterotrophic macro and megafauna in the CMSA. Trophic positions are estimated by nitrogen isotope ratios and feeding modes according to indicated references
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Appendix 1: Carbon and nitrogen isotopes ratios of heterotrophic macro and megafauna in the CMSA. Trophic positions are estimated by nitrogen isotope ratios and feeding modes according to indicated references

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Appendix 1: Carbon and nitrogen isotopes ratios of heterotrophic macro and megafauna in the CMSA. Trophic positions are estimated by nitrogen isotope ratios and feeding modes according to indicated references
Phylum SpecieFauna typeδ13CSDδ15NSDnTPSDFeeding modeReferencesSC
  1. Macro, macrofauna; Mega, megafauna. SD, Standart deviation; TP, Trophic position; n, samples number. SF, Suspension-feeder; DF, Deposit-feeder; C, Carnivore; G, Grazer; (?), Indeterminate feeding mode. SC, Station code on the map (see Fig. 1 and Table 1)

ProtozoaAllogromidae sp.Macro−16.411.611.8?9
 Globobulimina sp.Macro−23.6−9.61−4.4?7
 Protozoa sp.Macro−23.29.011.1?10
Porifera Axinella crinita Mega−17.921.614.8SFAndrade (1986)17
 Demospongidae sp. 1Mega−20.721.314.7SFRibes et al. (1999)23
 Porifera sp.Mega−16.811.411.8 SFRibes et al. (1999)17
Cnidaria Actiniaria sp. 1Mega−21.712.512.1SFOrejas (2001)10
 Actiniaria sp. 2Mega−17.917.813.6SFOrejas (2001)9
 Actinostola sp.Mega−15.619.514.1SFOrejas (2001)17
 Alcyoniidae sp.Mega−18.615.312.9SFOrejas (2001)8
 Anthozoa sp. 1Mega−18.0, −16.816.1, 17.623.4SFOrejas (2001)8
 Anthozoa sp. 2Mega−17.717.713.6SFOrejas (2001)8
 Anthozoa sp. 3Mega−22.811.511.8SFOrejas (2001)10
 Callogorgia sp.Mega−15.6, −13.410.3, 15.022.1SFOrejas (2001)9, 19
 Gorgoniidae sp.Mega−12.418.213.8SFOrejas (2001)16
 Hormathia sp.Mega−15.917.613.6SFOrejas (2001)23
 Paragorgia sp.Mega−22.411.111.7SFOrejas (2001)19
  Parascyphus repes Mega−21.711.911.9SFOrejas (2001)17
 Swiftia sp.Mega−17.43.714.21.852.60.5SFOrejas (2001)9, 10, 17, 19
NemerteaNemertea sp. 1Macro−16.715.413.0CLong & Poiner (1994)16
 Nemertea sp. 2Macro−21.05.810.1CLong & Poiner (1994)2
Anne lidaAmpharetidae sp. 1Macro−17.414.712.7DFFauchald & Jumars (1979)9
 Ampharetidae sp. 2Macro−18.5, −17.011.1, 12.821.9 DFFauchald & Jumars (1979)9
 Ampharetidae sp. 3Macro−19.414.312.6DFFauchald & Jumars (1979)1
 Ampharetidae sp. 4Macro−18.316.113.2DFFauchald & Jumars (1979)4
 Ampharetidae sp. 5Macro−17.214.112.6DFFauchald & Jumars (1979)10
 Amphinomidae sp. 1Macro−19.81.0-1-CFauchald & Jumars (1979)6
 Aricidea sp.Macro−19.4, −16.812.6, 16.522.7DFFauchald & Jumars (1979)1, 4
 Axiothella sp.Macro−16.91.617.80.543.70.1DFFauchald & Jumars (1979)1, 2, 4
 Capitellidae sp. 1Macro−19.34.115.30.232.90.1DFFauchald & Jumars (1979)6, 9
 Capitellidae sp. 2Macro−23.610.411.5DFFauchald & Jumars (1979)6
 Cirralutidae sp. 1Macro−21.1, −17.015.022.8DFFauchald & Jumars (1979)7, 8
 Chaetopteridae sp.Macro−14.217.613.6SFFauchald & Jumars (1979)1 5
 Chaetozone sp.Macro−19.41.614.62.532.70.7DFFauchald & Jumars (1979)1, 4
 Eteone sp.Macro−17.5, −15.615.8, 17.323.3CFauchald & Jumars (1979)3, 8
  Eunice pennata Mega−19.71.217.52.433.60.7CFauchald & Jumars (1979)9, 17
 Eunicidae sp. 1Mega−16.80.616.51.143.30.3CFauchald & Jumars (1979)8, 9
 Eunicidae sp. 2Mega−16.115.413.0CFauchald & Jumars (1979)9
 Exogone sp.Macro−17.41.116.60.333.30.1CFauchald & Jumars (1979)2, 4
 Fabrisabella sp.Macro−17.916.313.2SFFauchald & Jumars (1979)8
 Flabelligeridae sp.Macro−15.915.112.8DFFauchald & Jumars (1979)9
 Glyceridae sp.Macro−17.312.212.0CFauchald & Jumars (1979)9
 Harmothoe sp.Macro−16.618.914.0CFauchald & Jumars (1979)4
 Hesionidae sp.Macro−18.315.312.9CLong & Poiner (1994)9
 Lacydoniidae sp.Macro−17.58.310.9DFLong & Poiner (1994)8
 Lumbrineridae sp.Macro−18.71.215.81.193.10.3CFauchald & Jumars (1979)8, 9
  Maldane sarsi Mega−17.518.413.8DFFauchald & Jumars (197917
 Maldanidae sp. 1Macro−16.916.513.3DFFauchald & Jumars (1979)8
 Maldanidae sp. 2Macro−16.216.713.3DFFauchald & Jumars (1979)8
 Maldanidae sp. 3Macro−15.317.013.4DFFauchald & Jumars (1979)8
 Maldanidae sp. 4Macro−15.116.413.3DFFauchald & Jumars (1979)8
 Maldanidae sp. 5Macro−17.62.715.22.282.90.6DFFauchald & Jumars (1979)6, 8, 9, 10
 Maldanidae sp. 6Macro−15.915.913.1DFFauchald & Jumars (1979)8
 Maldanidae sp. 7Macro−13.817.413.5DFFauchald & Jumars (1979)9
 Maldanidae sp. 8Macro−16.114.912.8DFFauchald & Jumars (1979)10
 Mediomastus sp.Macro−16.60.116.00.743.10.2DFFauchald & Jumars (1979)1, 3, 4
 Nephtyidae sp.Macro−18.7-1-CFauchald & Jumars (1979)6
 Nereididae sp. 2Macro−27.7, −20.112.5, 14.722.4CFauchald & Jumars (1979)9
 Nereididae sp. 3Macro−16.718.914.0CFauchald & Jumars (1979)8
 Nereididae sp. 4Macro−18.115.012.8CFauchald & Jumars (1979)9
 Nereididae sp. 5Macro−16.618.213.8CFauchald & Jumars (1979)4
 Ninoe sp.Macro−18.22.217.30.333.50.1CFauchald & Jumars (1979)1, 4
 Odontosyllis sp.Macro−16.617.913.7CFauchald & Jumars (1979)4
 Oligochaeta sp.Macro−17.914.812.8CFauchald & Jumars (1979)8
 Orbiniidae sp.Macro−16.916.713.3DFFauchald & Jumars (1979)4
 Paraonidae sp.Macro−18.3, −17.011.8, 14.222.2DFFauchald & Jumars (1979)9
 Phyllodocidae sp. 1Macro−17.6-1-CFauchald & Jumars (1979)6
 Phyllodocidae sp. 2Macro−19.66.210.2CFauchald & Jumars (1979)8
 Phyllodocidae sp. 3Macro−19.1, −17.812.0, 16.122.5CFauchald & Jumars (1979)8, 9
 Polychaeta sp. 1Mega−18.3, −16.615.5, 17.723.2?17
 Polychaeta sp. 3Macro−18.815.713.0?9
 Polychaeta sp. 4Mega−14.219.414.1?16
 Polynoidae sp. 2Macro−17.51.916.31.252.70.8CFauchald & Jumars (1979)8, 9
 Prionospio sp.Macro−17.113.912.5DFFauchald & Jumars (1979)1
 Serpulidae sp.Mega−15.218.413.8SFFauchald & Jumars (1979)16
 Sphaerodoridae sp.Macro−20.314.412.7?15
 Syllidae sp. 1Macro−19.11.115.02.232.80.6CFauchald & Jumars (1979)8, 9, 10
 Syllidae sp. 2Macro−17.50.415.40.443.00.1CFauchald & Jumars (1979)8, 9
 Syllidae sp. 3Macro−17.913.812.5CFauchald & Jumars (1979)8
 Syllidae sp. 4Macro−19.115.312.9CFauchald & Jumars (1979)8
 Syllidae sp. 5Macro−16.8, −15.915.5, 14.022.8CFauchald & Jumars (1979)8
 Syllidae sp. 6Macro−19.6, −18.012.2, 15.822.5CFauchald & Jumars (1979)8, 9
 Syllidae sp. 7Macro−18.3, −16.617.5, 17.623.6CFauchald & Jumars (1979)1, 2
 Syllidae sp. 8Macro−18.013.312.3CFauchald & Jumars (1979)10
 Terebellidae sp. 1Macro−16.817.213.5DFFauchald & Jumars (1979)1
MolluscaBenthoctopus sp.Mega−16.1, −15.717.6, 17.923.6CQuiroga et al. (2009)3
 Cuspidaria sp.Mega−16.418.112.1SFQuiroga et al. (2009)9
 Cuspidaridae sp.Mega−16.53.012.52.933.70.9SFQuiroga et al. (2009)9, 10
 Chaetoderma sp.Macro−25.6, −22.13.8, 9.520.4SFAmbrose, (1993)1
  Fissidentalium majorinum Mega−13.518.113.8CQuiroga et al. (2009)9
 Fissidentalium sp.Mega−14.917.313.5CQuiroga et al. (2009)10
  Iothia megalodon Mega−16.618.513.9GWaren et al. (2011)17
 Iothia sp.Mega−17.1, −16.315.2, 15.122.9GWaren et al. (2011)8, 10
  Leptochiton americanus Mega−16.0, −15.718.3, 18.223.8CQuiroga et al. (2009)4
 Leptochiton sp.Mega−18.5, −8.919.1, 20.824.3CQuiroga et al. (2009)8, 9
  Limopsis marionensis Mega−15.318.013.7SFQuiroga et al. (2009)9
 Placiphorella sp.Mega−13.922.615.1CMclean, (1962)23
 Polyplacophora sp.Mega−5.219.614.2?16
 Punturella sp.Mega−16.518.713.9CQuiroga et al. (2009)16
 Scaphopoda sp.Mega−14.513.112.3CQuiroga et al. (2009)20
 Scissurella sp.Macro−16.114.712.7?8
 Stenosemus sp.Mega−14.419.514.1?16
  Zetela alphonsi Mega−15.317.514.7DFQuiroga et al. (2009)10
ArthropodaAega sp.Mega−15.518.813.9GThiel et al. (2003)17
 Amphipoda sp. 2Macro−19.412.712.1?15
 Calanoidea sp.Macro−20.3-1-?5
  Campylonotus semistriatus Mega−13.120.114.3CQuiroga et al. (2009)9
 Caprelloidea sp.Macro−17.712.112.0SFThiel et al. (2003)9
 Cirripedia sp. 1Mega−17.315.913.1SFFanelli et al. (2011)23
 Cirripedia sp. 2Mega−19.014.312.6SFFanelli et al. (2011)9
 Cirripedia sp. 3Mega−15.219.314.1SFFanelli et al. (2011)8
 Cumacea sp. 1Macro−22.47.110.5DFThiel et al. (2003)4
 Gammaridae sp.Macro−17.416.913.4CThiel et al. (2003)9
 Hyale sp.Macro−18.417.413.5CThiel et al. (2003)1
 Lepas sp.Mega−18.9, −12.412.0, 13.022.1SFFanelli et al. (2011)8, 10
  Munida propinqua Mega−17.417.113.4CQuiroga et al (2009)16
  Munidopsis quadrata Mega−14.9, −12.413.9, 16.122.8CChevaldonne & Olu, (1996)8
  Munidopsis trifida Mega−12.715.713.0CQuiroga et al. (2009)15
 Ostracoda sp.Macro−19.912.112.0SFKorniker (19789
 Scalpellidae sp.Mega−18.217.313.5SFFanelli et al. (2011)22
 Scalpellum sp.Mega−18.511.711.8SFFanelli et al. (2011)9
 Tanaidacea sp. 1Macro−17.116.713.3?8
 Tanaidacea sp. 2Macro−21.05.510.0?9
 Tanaidacea sp. 3Macro−19.414.712.7?2
 Tanaidacea sp. 4Macro−16.713.812.5?4
NematodaNematoda sp. 1Macro−22.0, −16.513.6, 14.122.5?9
 Nematoda sp. 3Macro−18.21.815.64.143.01.2?1, 2, 4
 Nematoda sp. 4Macro−19.4, −16.113.0, 16.822.8?2, 4
SipunculaSipunculidae sp. 1Macro−22.114.212.6DFMurina (1984)16
 Sipunculidae sp. 2Macro−24.06.310.3DFMurina (1984)14
 Sipunculidae sp. 3Macro−19.312.712.1DFMurina (1984)14
 Sipunculidae sp. 4Macro−18.313.912.5DFMurina (1984)19
 Sipunculidae sp. 5Macro−17.51.114.20.592.60.1DFMurina (1984)1, 2, 3, 4, 10
 Sipunculidae sp. 6Macro−16.6, −16.614.2, 13.322.5DFMurina (1984)9
BrachiopodaBrachiopoda sp. 1Mega−15.117.513.6SFPeck et al. (2005)9
 Brachiopoda sp. 2Mega−14.43.617.10.653.50.2SFPeck et al. (2005)8, 22
 Novocrania sp.Mega−14.520.414.4SFPeck et al. (2005)15
EchinodermataAsteroidea sp.Mega−16.916.613.3CQuiroga et al. (2009)8
  Astrodia tenuispina Mega−14.319.014.0CMortensen (1927)18
  Ophiomyxa vivipara Mega−13.213.512.4DFQuiroga et al. (2009)22
 Ophiuroidea sp. 2Mega−16.8, −14.714.3, 15.622.8?8
 Ophiuroidea sp. 3Mega−14.419.014.0?8
 Ophiuroidea sp.1Mega−11.314.312.6?22
 Psolus sp.Mega−14.617.413.5SFAndrade (1986)15
  Pteraster gibber Mega−21.917.913.7CMauzey et al. 196820
Chondrichthyes Bythaelurus canescens Mega−16.0, −13.017.2, 23.224.4CAcuna et al. (2010)9, 12
  Centroscyllium nigrum Mega−15.51.318.71.3123.90.4CPunzon & Herrera (2000)4, 8, 9, 11
Osteichthyes Antimora rostrata Mega−17.4, −17.314.9, 14.222.7CQuiroga et al. (2009)3
 Coelorhynchus cf. chilensisMega−14.220.014.3CLaptikhovsky (2005)9
  Coelorhynchus fasciatus Mega−15.419.714.2CLaptikhovsky (2005)11
 Coelorhynchus sp.Mega−15.0, −12.819.6, 19.624.2CLaptikhovsky (2005)8
  Coryphaenoides ariommus Mega−15.0, −14.920.8, 20.824.5CQuiroga et al. (2009)3
  Dissostichus eleginoides Mega−19.01.719.52.8104.10.8CMurillo et al. (2008)3, 4
 Hygophum sp.Mega−15.916.813.4CPakhomov et al. (1996)10
 Lampanyctus sp.Mega−15.118.914.0CUchikawa et al. (2008)10
  Lucigadus nigromaculatus Mega−15.619.514.2CStevens & Dunn (2011)9
 Macrouridae sp.Mega−17.020.914.6CStevens & Dunn (2011)3
 Macrurus holotrachysMega−16.4, −16.320.7, 21.124.6CQuiroga et al. (2009)3
 Myctophidae sp.Mega−16.218.213.8CUchikawa et al. (2008)10
  Nezumia pudens Mega−15.520.414.4CFanelli & Cartes (2010)8
 Stomiidae sp.Mega−16.420.014.3CSutton (2005)9