Abstract

Sellanes, J., Quiroga, E., and Neira, C. 2008. Megafauna community structure and trophic relationships at the recently discovered Concepción Methane Seep Area, Chile, ∼36°S. – ICES Journal of Marine Science, 65: 1102–1111.

The fauna, community composition, and trophic support of the newly discovered Concepción Methane Seep Area (CMSA) are compared with those at a nearby non-seep control. The assemblage of chemosymbiotic bivalves is defined by eight species, including the families Lucinidae, Thyasiridae, Solemyidae, and Vesicomyidae. Seep polychaetes are represented by Lamellibrachia sp. and two commensal species of the vesicomyid Calyptogena gallardoi. Although taxonomic analysis is still under way, most of the chemosymbiotic species seem to be endemics. The CMSA is a hotspot for non-seep benthic megafauna too; 101 taxa were present, but most of them are colonists or vagrants (i.e. not endemics of methane seeps). Isotope analysis supported the belief that non-symbiont-bearing species utilize photosynthetically fixed carbon, because they were isotopically distinct from the chemosymbiotic bivalve species present. It is our opinion that, at this site, which underlies one of the most productive coastal upwelling regions of the world, spatial heterogeneity and the availability of hard substratum, generated by the presence of authigenic carbonate crusts, are more important factors in attracting non-seep fauna than the availability of locally produced chemosynthetic food.

Introduction

The discovery of deep-water chemosynthetically fueled systems has been one of the most fascinating scientific findings of the past century (Spiess et al., 1980). Although only discovered two decades ago (Paull et al., 1984; Kennicut et al., 1985), cold-seep communities, those fueled by the emission of methane, have been identified at nearly 100 deep-water sites worldwide, on both active and passive continental margins, in the Atlantic, Pacific, and Indian Oceans, and in the Mediterranean Sea (Sibuet and Olu-Le Roy, 2002; Mazurenko and Soloviev, 2003; Levin, 2005), and most recently, at the shelf below the ice cap near the Antarctic Peninsula (Domack et al., 2005). However, just a small fraction of these sites have been characterized in terms of faunal communities (Levin, 2005). A key area to increase our understanding of seep biogeography is the SE Pacific coast off South America, because to date no studies have described the fauna comprehensively. An area of special interest is the Chilean margin, where, other than the fauna of the oxygen minimum zone (OMZ), little is known about the reducing ecosystems present. The OMZ benthos consists mainly of a community formed by the giant, sulphide-oxidizing bacteria Thioploca (Gallardo, 1977), which carpets the shelf sediments that are impinged by the SE Pacific oxygen minimum layer. However, the realm beyond the shelf break off the Chilean margin has remained mostly unexplored for chemosynthetic systems. Indeed, there have been only a few reports of chemosynthetic taxa off South American coasts: off NE Brazil (e.g. Calyptogena birmani; Domaneschi and Lopes, 1990), off Uruguay (e.g. Lamellibrachia victori; Mañé-Garzón and Montero, 1986), off Chile (e.g. Ectenagena australis; Stuardo and Valdovinos, 1988), and the Yaquina Basin methane seeps off Peru (Olu et al., 1996) are the only ones with detailed biological characterization to date.

Several aspects of the Chilean margin suggest the existence of extensive methane-seep communities: (i) the report of vast gas hydrate fields extending from 35°S to 45°S (Morales, 2003); (ii) the presence of an active subduction front with a well-developed accretionary prism and suggesting fluid expulsion from the sediment (Lagabrielle et al., 2004); and (iii) the early description of the chemosymbiotic clam, E. australis, from ∼1400 m after incidental collection of two specimens by bottom longliners (Stuardo and Valdovinos, 1988).

Based on dredged chemosymbiotic clam fragments and carbonate blocks, the first active seep site off the Chilean coast was recently discovered, the Concepción Methane Seep Area (CMSA; ∼36°S; Sellanes et al., 2004). This study describes the fauna of this southernmost South American methane-seep area, and compares the roles of chemosynthetic and photosynthetic nutrition in a deep-water seep that underlies one of the most productive photic zones in the world. In this context, we aim to characterize the taxonomic composition of megafaunal communities, including both chemosymbiotic and accompanying non-chemosymbiotic species, and to assess the utilization of chemosynthesis-based food sources by members of the cold-seep community based on C and N stable isotope analysis.

Material and methods

Study area

The CMSA is located 72 km northwest of Concepción Bay (36°22′S 73°73′W), on the mid-slope (740–870 m water depth), and on one side of two adjacent mounds separated by a shallow depression (Figure 1). Previous piston-core deployments have found large gas hydrate deposits with carbon isotopic values of −62.8 ± 1.0‰ for both the hydrates themselves and sedimentary porewater (Coffin et al., 2006); this value is indicative of a biogenic origin of the methane (Ussler et al., 2003). There are abundant blocks formed by carbonate-cemented mud, i.e. mud breccia, containing shell fragments of at least two species of clam known to harbour chemosymbiotic endosymbionts, e.g. a vesicomyid and a solemyid (Figure 2; Sellanes et al., 2004). Previous studies have also reported dead vesicomyids and other species of chemosymbiotic clam (e.g. Lucinoma anemiophila, Thyasira methanophila, and Conchocele sp.; Sellanes and Krylova, 2005).

Figure 1.

Study area off Concepción Bay, Central Chile. The triangle indicates trawls where evidence of active methane seepage was collected (carbonate blocks, live chemosymbiotic clams, and shell fragments). The star indicates the position in which shallow subsurface gas hydrates have been observed.

Figure 1.

Study area off Concepción Bay, Central Chile. The triangle indicates trawls where evidence of active methane seepage was collected (carbonate blocks, live chemosymbiotic clams, and shell fragments). The star indicates the position in which shallow subsurface gas hydrates have been observed.

Figure 2.

Typical carbonate block collected at the study area. Cemented valves of vesicomyids are also visible. Scale bar = 5 cm.

Figure 2.

Typical carbonate block collected at the study area. Cemented valves of vesicomyids are also visible. Scale bar = 5 cm.

A control non-seep site was also sampled to compare the megafaunal composition of the CMSA with the typical bathyal fauna at a similar depth. This site, situated at 36°32.54′S 73°40.05′W, 798 m deep, and 27 km south of the CMSA, was chosen based on faunal information gathered during a RV “Sonne” cruise (site GeoB 7162; Hebbeln et al., 2001). An underwater video transect, a piston-corer deployment, and trawled megafauna did not show any evidence of methane-seep activity in the area. Indeed, analysis of the piston corer showed that the upper 345 cm of the sediment at this non-seep site consisted largely of hemipelagic clays (Hebbeln et al., 2001).

Sample collection and analysis

Sampling was conducted on board the Chilean Navy’s RV “Vidal Gormáz” during October 2004 (VG–04 cruise) and September 2006 (SeepOx cruise), and on the RV “Sonne” (a few samples; Table 1). Samples were collected by an Agassiz trawl (mouth opening 1.5 × 0.5 m, mesh size 10 × 10 mm in the codend), in 20-min hauls. Animals were sorted from the non-biological material and preserved on board using appropriate methods for later analysis (e.g. frozen, buffered 10% seawater formalin, glutaraldehyde, and absolute ethanol). Only trawls in which evidence of chemosynthetic activity was observed (e.g. carbonates, shell fragments, or living chemosymbiotic clams) were used for the analysis. No estimates of biomass or abundance were attempted because of the hardness of the substratum and the consequent inadequacy of the collection method for quantitative calculations. Additionally, the collection of large volumes of carbonate blocks (500–1000 kg at each haul) made complete sorting of the samples impractical. However, an indication of the relative frequency of occurrence of each species, based on its relative abundance, was recorded as follows: (i) abundant, present in all hauls and in considerable quantities (e.g. >10 specimens), (ii) common, present in 50% or more of the hauls and sometimes in considerable numbers, (iii) occasional, present in <50% of hauls, in general in small quantities, and (iv) rare, just a few specimens collected in one or two hauls.

Table 1.

Initial position of trawls (Agassiz trawls, AGT) during VG–04, SeepOx, and SO–156 cruises at the CMSA and the control non-seep site. Observations on the occurrence of chemosymbiotic fauna for AGTs at the seep site are also provided.

Cruise Gear Latitude S Longitude W Depth (m) Observations* 
VG–04 AGT 6 36°21.75′ 73°43.55′ 726–865 Cgl,d, V1d, Ccd 
 AGT 7 36°21.64′ 73°43.57′ 865–926 Cgl,d, V2l, Cxd, Axl, Tml, Lbd 
 AGT 8 36°21.80′ 73°43.10′ 708–854 Cgd, V1d, Tml,d 
 AGT 9 36°21.90′ 73°43.21′ 713–850 Cgl,d, V1l,d, Lbd 
 AGT 10 36°22.68′ 73°42.46′ 708–709 Axd, Lad 
 AGT 13 36°21.91′ 73°43.21′ 728–843 Cgl,d, V1d, Axd, Lad, Tml,d 
SeepOx AGT 6–3 36°21.18′ 73°43.89′ 919–891 Cgl,d, V2d, Tmd 
 AGT 6–5 36°21.60′ 73°43.88′ 728–885 Cgd, V1d, Tmd 
 AGT 6–8 36°21.90′ 73°43.21′ 710–870 Cgl,d, V1d, Lbl,d 
 AGT 7–1 36°32.05′ 73°45.02′ 879–880 Control, non-seep site 
 AGT 7–2 36°32.54′ 73°40.52′ 817–820 Control, non-seep site 
SO–156 AGT 7162 36°32.54′ 73°45.72′ 798–782 Control non-seep site 
Cruise Gear Latitude S Longitude W Depth (m) Observations* 
VG–04 AGT 6 36°21.75′ 73°43.55′ 726–865 Cgl,d, V1d, Ccd 
 AGT 7 36°21.64′ 73°43.57′ 865–926 Cgl,d, V2l, Cxd, Axl, Tml, Lbd 
 AGT 8 36°21.80′ 73°43.10′ 708–854 Cgd, V1d, Tml,d 
 AGT 9 36°21.90′ 73°43.21′ 713–850 Cgl,d, V1l,d, Lbd 
 AGT 10 36°22.68′ 73°42.46′ 708–709 Axd, Lad 
 AGT 13 36°21.91′ 73°43.21′ 728–843 Cgl,d, V1d, Axd, Lad, Tml,d 
SeepOx AGT 6–3 36°21.18′ 73°43.89′ 919–891 Cgl,d, V2d, Tmd 
 AGT 6–5 36°21.60′ 73°43.88′ 728–885 Cgd, V1d, Tmd 
 AGT 6–8 36°21.90′ 73°43.21′ 710–870 Cgl,d, V1d, Lbl,d 
 AGT 7–1 36°32.05′ 73°45.02′ 879–880 Control, non-seep site 
 AGT 7–2 36°32.54′ 73°40.52′ 817–820 Control, non-seep site 
SO–156 AGT 7162 36°32.54′ 73°45.72′ 798–782 Control non-seep site 

*Cg, Calyptogena gallardoi; V1, vesicomyid gen. sp. 1; V2, vesicomyid gen. sp. 2; Cx, Calyptogena sp.; Ax, Acharax sp.; Tm, Thyasira methanophila; Cc, Conchocele sp.; La, Lucinoma anemiophila; Lb, Lamellibrachia sp.; lliving specimens; ddead or shell fragments.

Samples for bottom water particulate organic matter (POM) were collected at the CMSA using a Rosette with 12 × 8 l Niskin bottles. For each sample, ∼2 l of water was pre-sieved through a 63-µm mesh to remove zooplankton and large detrital particles, then filtered onto pre-combusted (500°C for 4 h) Whatman GF/F filters (nominal 0.7 µm pore size).

Stable isotope analysis

Stable C and N isotope signatures were analysed for animals, sedimentary organic matter (SOM), bottom-water-suspended POM, and randomly collected potential food sources (e.g. remains of macroalgae, probably Macrocystis pyrifera, at the control site). Additional muscle tissue samples of Patagonian toothfish (Dissostichus eleginoides), a large predatory fish known to be present at the seep site but difficult to collect by trawling, were obtained from fish caught by artisanal fishers operating at the CMSA. Samples were frozen (−20°C) and later dried at 60°C overnight. After being ground to a fine powder using an agate mortar, samples were treated with a 1% solution of PtCl2 to remove inorganic carbon. Because of the elevated lipid content of D. eleginoides, small pieces of tissue (<1 g) were rinsed with distilled water, air-dried, soaked in a 1:1 chloroform:methanol solution three times, then rinsed with distilled water to remove lipids before stable isotope analyses (Beaudoin et al., 2001). This lipid removal does not produce significant δ13C and δ15N shifts in lipid-free samples (Sotiropoulos et al., 2004).

Isotope composition was analysed in the laboratory of R. Lee (School of Biological Sciences, Washington State University) by a Eurovector elemental analyser (Milan, Italy) coupled to a Micromass Isoprime isotope ratio mass spectrometer (Manchester, UK). Stable isotope ratios are reported in the δ notation as the deviation from standards (Pee Dee Belemnite for δ13C and atmospheric N 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.

Results

Chemosymbiotic fauna

The chemosymbiotic assemblage of the CMSA was dominated by eight species of bivalve (Figure 3). Of the Vesicomyidae, Calyptogena gallardoi was the most frequently collected. Three other unresolved vesicomyids were present too: a large and slender species (gen. sp. 1), measuring up to 180-mm long, a species of medium size, with an elliptical outline and adherent periostracum (gen. sp. 2), and another species of the genus Calyptogena, similar to C. gallardoi in appearance, but with a subcircular shell outline (Figure 3). Other chemosymbiotic bivalve families included the Lucinidae (L. anemiophila; Holmes et al., 2005), Thyasiridae (T. methanophila; Oliver and Sellanes, 2005, and Conchocele sp.), and Solemyidae (Acharax sp.). Although more living specimens of Conchocele sp. and Acharax sp. are needed for proper taxonomic studies, upon initial examination they do not correspond to species previously described. Indeed, it is the first time that the genus Conchocele has been reported in the SE Pacific (Oliver and Sellanes, 2005).

Figure 3.

Chemosymbiotic bivalve assemblage of the CMSA: (a) vesicomyid gen. sp. 1, (b) vesicomyid gen. sp. 2, (c) Calyptogena gallardoi, (d) Calyptogena sp., (e) Thyasira methanophila, (f) Conchocele sp., (g) Lucinoma anemiophila, and (h) Acharax sp. Scale bar = 2 cm.

Figure 3.

Chemosymbiotic bivalve assemblage of the CMSA: (a) vesicomyid gen. sp. 1, (b) vesicomyid gen. sp. 2, (c) Calyptogena gallardoi, (d) Calyptogena sp., (e) Thyasira methanophila, (f) Conchocele sp., (g) Lucinoma anemiophila, and (h) Acharax sp. Scale bar = 2 cm.

Three polychaete species were sampled successfully, including one chemosymbiotic and two commensal taxa. Six living Lamellibrachia spp. (Siboglinidae), and several unoccupied tubes up to 130-cm long, were collected. A few C. gallardoi (∼10%) hosted commensal polychaetes belonging to two different families, one to the Nautiliniellidae (Shinkai sp.) and the other to the Antonbruunidae (Antonbruunia sp.). To our knowledge, this is the first time that two species of commensal polychaete have been reported for a single vesicomyid species. These species are novel and are currently being described.

Heterotrophic fauna

Of the 101 non-chemosymbiotic megafaunal species observed at the CMSA (Table 2), an onuphid polychaete (Hyalinoecia sp.), a solenocerid shrimp (Haliporoides diomedeae), and many species of cnidarians, gastropods (Bathybembix, Miomelon, and Homalopoma), annelids, crustaceans, and echinoderms were particularly abundant. Macrourids (grenadiers or rattails) were also common (Table 2). All 24 species collected at the control site were also present at the CMSA, but none was as abundant at the control site as at the CMSA. Hyalinoecia sp., H. diomedeae, and the elasmobranchs Halaelurus canescens and Bathyraja sp., as well as the rattail Coelorinchus fasciatus, were the most conspicuous species at the control site.

Table 2.

Species collected at the CMSA and control non-seep sites.

Taxa Seep endemic CMSA Non-seep 
PORIFERA    
   gen. sp. Y/N – 
CNIDARIA    
Anthozoa    
 Alcyonaria    
  Gorgonacea    
   Paragorgia sp. – 
   Callogorgia sp. – 
   Swiftia sp. – 
   gen. sp. – 
 Zoantharia    
  Actinaria    
   Actinostola sp. – 
   Coralliomorphus sp. – 
   Hormathia sp. – 
   gen. sp. – 
  Scleractinia    
  Cariophyllidae    
   Bathycyatus chilensis – 
   Caryophyllia huinayensis – 
  Flabellidae    
   Flabellum apertum – 
MOLLUSCA    
Polyplacophora    
  Leptochitonidae    
   Leptochiton americanus – 
  Ischnochitonidae    
   Stenosemus exaratus – 
  Mopaliidae    
   Placiphorella atlantica – 
Gastropoda    
  Neolepetopsidae    
   Bathylepeta sp. Y/N – 
  Fissurellidae    
   Puncturella sp. 1 Y/N – 
   Puncturella sp. 2 
  Trochidae    
   Bathybembix macdonaldi 
   Margarites huloti Y/N – 
   Zetela alphonsi – 
   Calliotropis sp. – 
  Calliostomatidae    
   Calliostoma chilena  
   Calliostoma crustulum – 
  Turbinidae    
   Homalopoma panamense – 
  Naticidae    
   Natica sp. 
  Ranellidae    
   Fusitriton magellanicus – 
  Muricidae    
   Coronium cf. wilhelmense – 
   Pagodula concepcionensis – 
   Trophon ceciliae – 
   Trophon condei – 
  Buccinidae    
   Kryptos explorator – 
  Volutidae    
   Miomelon philippiana 
  Turridae    
   Aforia cf. goniodes 
   gen. sp. 1 – 
   gen. sp. 2 – 
Bivalvia    
  Nuculidae    
   Ennucula grayi 
  Solemyidae    
   Acharax sp. – 
  Limopsidae    
   Limopsis ruizana – 
  Lucinidae    
   Lucinoma anemiophila – 
  Thyasiridae    
   Thyasira methanophila – 
   Conchocele sp. – 
  Vesicomyidae    
   Calyptogena gallardoi – 
   Calyptogena sp. – 
   gen. sp. 1 – 
   gen. sp. 2 – 
Scaphopoda    
  Dentalidae    
   Fissidentalium majorinum 
Cephalopoda    
  Octopodidae    
   Benthoctopus sp. – 
  Sepiolidae    
   Semirossia patagonica – 
ANNELIDA    
Polychaeta    
  Onuphidae    
   Hyalinoecia sp. 
  Eunicidae    
   Eunice cf. magellanica 
   Eunice sp. – 
  Aphroditidae    
   Aphrodite longirostris – 
  Sabellidae    
   gen. sp. – 
  Lumbrineridae    
   gen. sp. – 
  Antobruunidae    
   Antonbruunia sp. – 
  Nautiliniellidae    
   Shinkai sp. – 
  Siboglinidae    
   Lamellibrachia sp. – 
CRUSTACEA    
Cirripedia    
 Thoracica    
  Scalpellidae    
   Arcoscalpellum sp. – 
   Scalpellum projectum – 
Decapoda    
 Dendrobranchiata    
  Solenoceridae    
   Haliporoides diomedeae 
 Pleocyemata    
  Oplophoridae    
   Acantephyra pelagica – 
   Oplophorus novaezeelandiae – 
  Campylonotidae    
   Campylonotus semistriatus 
  Crangonidae    
   Paracrangon areolata – 
   Sclerocrangon atrox – 
  Polychelidae    
   Stereomastis sculpta 
  Galatheidae    
   Munidopsis quadrata – 
   Munidopsis trifida – 
   Munida curvipes – 
   Munida propinqua – 
  Atelecyclidae    
   Trichopeltarion corallinus – 
   Trichopeltarion hystricosus – 
  Lithodidae    
   Lithodes turkayi – 
   Paralomis sp. – 
Isopoda    
  Cirolanidae    
   Cirolana sp. – 
   Aega sp. – 
BRACHIOPODA    
   Liothyrella cf. scotti – 
   gen. sp. – 
ECHINODERMATA    
Crinoidea    
   Solanometra sp. – 
Asteroidea    
  Ctenodiscididae    
   Ctenodiscus australis – 
  Pterasteridae    
   Hymenaster sp. – 
  Solasteridae    
   Solaster regularis – 
  Zoroasteridae    
   Doraster qawashqari 
  Goniasteridae    
   Ceramaster patagonicus – 
   Hippasteria hyadesi – 
   gen. sp. 1 
   gen. sp. 2 – 
Ophiuroidea    
  Gorgonocephalidae    
   Gorgonocephalus chilensis – 
  Asteronychidae    
   Asteronyx loveni – 
   Astrodia tenuispina – 
   Astrodia sp. – 
  Ophiuridae    
   Ophiura carinata 
   Stegophiura sp. – 
  Ophiolepididae    
   Ophiomusium biporicum – 
   Ophiomusium lymani – 
Echinoidea    
  Schizasteridae    
   Tripylaster sp. 
  Phymosomatidae    
   Phormosoma sp. 
Holothuroidea    
   gen. sp. – 
SIPUNCULIDA    
   gen. sp. 
CHORDATA    
Chondricthyes    
  Dalatiidae    
   Centroscyllium granulatum – 
  Scyliorhinidae    
   Halaelurus canescens 
  Rajidae    
   Bathyraja sp. 
Actinopterygii    
  Psychrolutidae    
   Psychrolutes sio – 
  Macruridae    
   Coryphaenoides ariommus – 
   Coelorinchus fasciatus 
   Coelorinchus chilensis – 
  Moridae    
   Antimora rostrata 
  Zoarcidae    
   Bothrocara alalongum 
  Notocanthidae    
   Notacanthus sexspinis – 
  Alepocephalidae    
   gen. sp. – 
Taxa Seep endemic CMSA Non-seep 
PORIFERA    
   gen. sp. Y/N – 
CNIDARIA    
Anthozoa    
 Alcyonaria    
  Gorgonacea    
   Paragorgia sp. – 
   Callogorgia sp. – 
   Swiftia sp. – 
   gen. sp. – 
 Zoantharia    
  Actinaria    
   Actinostola sp. – 
   Coralliomorphus sp. – 
   Hormathia sp. – 
   gen. sp. – 
  Scleractinia    
  Cariophyllidae    
   Bathycyatus chilensis – 
   Caryophyllia huinayensis – 
  Flabellidae    
   Flabellum apertum – 
MOLLUSCA    
Polyplacophora    
  Leptochitonidae    
   Leptochiton americanus – 
  Ischnochitonidae    
   Stenosemus exaratus – 
  Mopaliidae    
   Placiphorella atlantica – 
Gastropoda    
  Neolepetopsidae    
   Bathylepeta sp. Y/N – 
  Fissurellidae    
   Puncturella sp. 1 Y/N – 
   Puncturella sp. 2 
  Trochidae    
   Bathybembix macdonaldi 
   Margarites huloti Y/N – 
   Zetela alphonsi – 
   Calliotropis sp. – 
  Calliostomatidae    
   Calliostoma chilena  
   Calliostoma crustulum – 
  Turbinidae    
   Homalopoma panamense – 
  Naticidae    
   Natica sp. 
  Ranellidae    
   Fusitriton magellanicus – 
  Muricidae    
   Coronium cf. wilhelmense – 
   Pagodula concepcionensis – 
   Trophon ceciliae – 
   Trophon condei – 
  Buccinidae    
   Kryptos explorator – 
  Volutidae    
   Miomelon philippiana 
  Turridae    
   Aforia cf. goniodes 
   gen. sp. 1 – 
   gen. sp. 2 – 
Bivalvia    
  Nuculidae    
   Ennucula grayi 
  Solemyidae    
   Acharax sp. – 
  Limopsidae    
   Limopsis ruizana – 
  Lucinidae    
   Lucinoma anemiophila – 
  Thyasiridae    
   Thyasira methanophila – 
   Conchocele sp. – 
  Vesicomyidae    
   Calyptogena gallardoi – 
   Calyptogena sp. – 
   gen. sp. 1 – 
   gen. sp. 2 – 
Scaphopoda    
  Dentalidae    
   Fissidentalium majorinum 
Cephalopoda    
  Octopodidae    
   Benthoctopus sp. – 
  Sepiolidae    
   Semirossia patagonica – 
ANNELIDA    
Polychaeta    
  Onuphidae    
   Hyalinoecia sp. 
  Eunicidae    
   Eunice cf. magellanica 
   Eunice sp. – 
  Aphroditidae    
   Aphrodite longirostris – 
  Sabellidae    
   gen. sp. – 
  Lumbrineridae    
   gen. sp. – 
  Antobruunidae    
   Antonbruunia sp. – 
  Nautiliniellidae    
   Shinkai sp. – 
  Siboglinidae    
   Lamellibrachia sp. – 
CRUSTACEA    
Cirripedia    
 Thoracica    
  Scalpellidae    
   Arcoscalpellum sp. – 
   Scalpellum projectum – 
Decapoda    
 Dendrobranchiata    
  Solenoceridae    
   Haliporoides diomedeae 
 Pleocyemata    
  Oplophoridae    
   Acantephyra pelagica – 
   Oplophorus novaezeelandiae – 
  Campylonotidae    
   Campylonotus semistriatus 
  Crangonidae    
   Paracrangon areolata – 
   Sclerocrangon atrox – 
  Polychelidae    
   Stereomastis sculpta 
  Galatheidae    
   Munidopsis quadrata – 
   Munidopsis trifida – 
   Munida curvipes – 
   Munida propinqua – 
  Atelecyclidae    
   Trichopeltarion corallinus – 
   Trichopeltarion hystricosus – 
  Lithodidae    
   Lithodes turkayi – 
   Paralomis sp. – 
Isopoda    
  Cirolanidae    
   Cirolana sp. – 
   Aega sp. – 
BRACHIOPODA    
   Liothyrella cf. scotti – 
   gen. sp. – 
ECHINODERMATA    
Crinoidea    
   Solanometra sp. – 
Asteroidea    
  Ctenodiscididae    
   Ctenodiscus australis – 
  Pterasteridae    
   Hymenaster sp. – 
  Solasteridae    
   Solaster regularis – 
  Zoroasteridae    
   Doraster qawashqari 
  Goniasteridae    
   Ceramaster patagonicus – 
   Hippasteria hyadesi – 
   gen. sp. 1 
   gen. sp. 2 – 
Ophiuroidea    
  Gorgonocephalidae    
   Gorgonocephalus chilensis – 
  Asteronychidae    
   Asteronyx loveni – 
   Astrodia tenuispina – 
   Astrodia sp. – 
  Ophiuridae    
   Ophiura carinata 
   Stegophiura sp. – 
  Ophiolepididae    
   Ophiomusium biporicum – 
   Ophiomusium lymani – 
Echinoidea    
  Schizasteridae    
   Tripylaster sp. 
  Phymosomatidae    
   Phormosoma sp. 
Holothuroidea    
   gen. sp. – 
SIPUNCULIDA    
   gen. sp. 
CHORDATA    
Chondricthyes    
  Dalatiidae    
   Centroscyllium granulatum – 
  Scyliorhinidae    
   Halaelurus canescens 
  Rajidae    
   Bathyraja sp. 
Actinopterygii    
  Psychrolutidae    
   Psychrolutes sio – 
  Macruridae    
   Coryphaenoides ariommus – 
   Coelorinchus fasciatus 
   Coelorinchus chilensis – 
  Moridae    
   Antimora rostrata 
  Zoarcidae    
   Bothrocara alalongum 
  Notocanthidae    
   Notacanthus sexspinis – 
  Alepocephalidae    
   gen. sp. – 

Organisms endemic to seeps (Y) or not (N), and relative abundance: A, abundant; C, common; O, occasional; R, rare; –, not present.

Stable isotope signatures

Usually, chemosymbiotic organisms were isotopically distinct from the heterotrophic fauna (Figure 4, Appendix). Vesicomyids had the lowest δ13C and δ15N signatures, ranging from −36.2 to −35.4‰ for δ13C, and from 2.9 to 4.8‰ for δ15N, whereas values for 15N of Thyasira methanophila15N = 10.0‰) and for δ13C of Lamellibrachia sp. (δ13C = −22.9‰) were close to the range of POM and SOM.

Figure 4.

Dual isotope plot of δ13C and δ15N (mean ± s.d.) of chemosynthetic invertebrates, non-chemosynthetic food sources, and secondary consumers (invertebrates and fish) at the CMSA (white dots) and control non-seep sites (black dots). *See the text for explanation on the comparatively heavy 13C values of Lamellibrachia sp.

Figure 4.

Dual isotope plot of δ13C and δ15N (mean ± s.d.) of chemosynthetic invertebrates, non-chemosynthetic food sources, and secondary consumers (invertebrates and fish) at the CMSA (white dots) and control non-seep sites (black dots). *See the text for explanation on the comparatively heavy 13C values of Lamellibrachia sp.

Isotopic signatures did not differentiate the non-symbiont-bearing fauna between the control and CMSA sites (Figure 4). At the CMSA, heterotrophic fauna δ13C ranged from −19.8 to −11.0‰, and δ15N from 12.6 to 23.5‰. Isotopic signatures of the heterotrophic fauna at the control site were within this range (Appendix). This suggests that at both CMSA and control sites, the primary organic food sources are basically the same, most probably POM and SOM. However, some top predators at the CMSA displayed slightly lighter δ13C values than lower trophic level consumers (Appendix). These include the Patagonian toothfish (δ13C = −18.6‰), the octopus Benthoctopus sp. (δ13C = −17.8‰), and the morid Antimora rostrata13C = −17.4‰), the latter also with a relatively low δ15N (15.0‰). Antimorarostrata collected at the control site displayed heavier isotopic signatures for both isotopes (δ13C = −16.0‰ and δ15N = 20.1‰).

Discussion

Chemosymbiotic faunal composition

As cold-seep exploration at the SE Pacific margin is just starting, and more seep sites are expected to be discovered there, it is still too early to discuss the degree of endemicity of the CMSA chemosymbiotic fauna, or to consider patterns of latitudinal or depth zonation. However, none of the chemosynthetic species collected here is apparently shared with similar communities off Peru (5–6°S), the closest seep area so far described (∼3500 km to the north). Peruvian seeps have been reported from 2630 to 5140 m deep, with their fauna distributed as a function of depth. Their chemosymbiotic fauna are constituted by three vesicomyids, a solemyid bivalve of the genus Acharax, and a “pogonophoran” (Olu et al., 1996). The vesicomyid Calyptogena goffrediae was recently described, and it resembles C. gallardoi in shape and size, but differs in having a shallower escutcheon, a more curved beak, and a more expanded anterodorsal shell region (Krylova and Sahling, 2006). The other two vesicomyids observed still remain undescribed.

Our work has produced the first record of living siboglinids for the Chilean margin. Tubeworms associated with seep sites have been also reported for the Peruvian margin (Olu et al., 1996), but no detail of their taxonomic status was given. The only species of siboglinid reported for the Eastern Pacific is Lamellibrachiabarhami from the continental slope of southern California and Oregon, the median valley of the Juan de Fuca Ridge, San Clemente Basin, and Monterey Bay, at depths of 600–2400 m (Schulze, 2003), and from the Costa Rica margin, ∼8 to 10°N at depths of 1000–2400 m (Mau et al., 2006). However, according to a Cytochrome C Oxidase Subunit 1 (CO1) analysis of the CMSA species, and comparison with other representatives of the genus, the Chilean species is closer to Lamellibrachia luymesi. This last species, which inhabits the upper slope of the Gulf of Mexico (<1000 m), has a 3% sequence divergence with the CMSA species, suggesting that it is indeed different (C. Fisher and K. Nelson, pers. comm.).

Our limited knowledge of the Chilean margin seep fauna also suggests that its bivalve-dominated chemosymbiotic community structure is similar to the better-studied counterpart at Monterey Bay on the Northeast Pacific upper slope (∼39°N, 500–1000 m). As an example, the most common CMSA vesicomyids, C. gallardoi and vesicomyid gen. sp. 1, morphologically resemble Calyptogenapacifica and Calyptogenakilmeri, respectively, which are the dominant species at Monterey seep habitats (Goffredi et al., 2004). Three additional vesicomyids have been reported for Monterey Bay, but in lesser abundance, and two less abundant vesicomyids were also observed at the CMSA. Moreover, as well as the fauna reported in Mediterranean mud volcanoes (Olu-Le Roy et al., 2004), the fauna of the CMSA seems to include symbiotic species that are not restricted to seeps but adapted to organic rich environments (e.g. oxygen-deficient settings), such as thyasirids and lucinids. The proximity of an intense OMZ, where lucinid and thyasirid bivalves are often common (Levin, 2003), may contribute to the adaptation, diversity, and evolution of these groups within seeps. We do not know yet whether all the habitat patch types typical of the Alaska, Oregon, California, Costa Rica, and Peru seeps (mats of filamentous sulphur bacteria, Calyptogena, Acharax beds, serpulid beds, vestimentiferan aggregations, and siboglinid fields) are present off Chile, or whether there are novel habitat configurations. Finally, it is noteworthy that, of all the known eastern Pacific seeps, only those off Costa Rica support mussel beds (Mau et al., 2006), despite mytilids being common at eastern Pacific vent sites, such as the Galapagos Spreading Centre and the East Pacific Rise (Van Dover, 2000). Vesicomyids appear to replace mussels as the dominant biomass at the well-studied eastern Pacific seeps (Levin, 2005).

Megafaunal community structure at the CMSA vs. the control non-seep site

Although we did not attempt to calculate faunal densities, owing to the roughness of the seep-site terrain, it was evident that our site was clearly richer in species and that fauna was more abundant than at the control non-seep site. Only 24 megafauna species were observed at the non-seep site, and all were also present at the CMSA (Table 2). At the control site, the solenocerid shrimp H. diomedeae was dominant, along with the polychaete Hyalinoecia sp. and macrourids, but always in lesser numbers than at the seep site. The reduced species richness of the control site can in part be explained by the absence of hard substratum, which resulted in a virtual absence of sessile fauna, mainly cnidarians (e.g. gorgonians) and their associated fauna (e.g. brittlestars and galatheid crustaceans). The role of deep-water corals in structuring benthic communities is widely recognized as providing a food source, a perch for suspension-feeders, and protection from predation (Krieger and Wing, 2002).

When compared with other seep sites worldwide, the CMSA epibenthos species number ranks among the highest reported. Just 25 species have been reported for Mediterranean mud volcanoes (Olu-Le Roy et al., 2004), 83 taxa for the clam-bed and microbial-mat habitats on the northern California slope (Levin et al., 2003), 86 taxa for the San Clemente cold seep (Baco and Smith, 2003), and 66 species associated with vestimentiferan aggregations in the Gulf of Mexico (Bergquist et al., 2003). However, due to each of these studies only examining a subset of the total fauna (i.e. some were more focused on the macrofauna and others on the megafauna), and methodological approaches differing, comparisons should be made with caution. Nevertheless, ecosystem-wide species counts are likely to be much higher, because it is expected that the CMSA also hosts a rich meiofaunal and macrofaunal assemblage. Once assessed, these groups will probably increase the species number of animals associated with our site considerably.

According to Carney (1994), colonists are heterotrophic species attracted to vent or seep sites by the aggregation of chemo-autotrophically derived organic matter, endemics are species never found outside reducing environments, and vagrants occur uniformly within and outside vents and seeps. The very limited knowledge of Chilean background bathyal fauna prevents us evaluating whether the non-chemosymbiotic fauna we found are seep endemics, although most of them seem to be colonists or vagrants. Many of the species we collected, like Pagodula concepcionensis, Otukaia crustulum, and Margarites huloti, are new to science (Houart and Sellanes, 2006; Vilvens and Sellanes, 2006). Representatives of some of these genera have been reported for seep sites off Japan (e.g. Margarites shinkai). However, excluding the antonbruunid and nautiliniellid polychaetes, commensal of C. gallardoi, no other species of non-chemosymbiotic fauna endemic of seeps (e.g. provannid gastropods, alvinocarid shrimps), were found. Hence, the CMSA assemblage shares some characteristics of the shallow-water methane seeps off California (Levin et al., 2000) and the North Sea (Dando et al., 1991), which have dense faunal populations but few seep endemics. This contrasts with observations in the Gulf of Mexico, where relatively high levels of faunal endemism are tightly associated with vestimentiferan aggregations (MacAvoy et al., 2005).

Primary sources driving the heterotrophic foodweb

Except Lamellibrachia, chemosymbiotic animal signatures did not overlap with photosynthetic or sediment organic carbon isotopic signatures. Sediment and suspended matter organic carbon isotopic values were nearly in the range for photosynthetically fixed material (δ13C from −20.2 to −23.47‰; Appendix). There were also relatively high organic carbon (2.6%) and chlorophyll a (4.07 µg g−1) contents in the control-site sediments (Quiroga et al., in press). This information, along with sediment isotopic signatures, suggests that a large fraction of the partially undegraded phytodetritus reaches the mid-slope seabed off Concepción. Moreover, trawled fragments of Macrocystis at the control site also indicate that inputs of other photosynthetic sources are present (Appendix). Chemosymbiotic animals showed δ13C values lighter than −35‰, except Lamellibrachia sp., with a δ13C of −22.8‰. Similar 13C-enriched values have been reported for other siboglinids (e.g. −20.1‰ for L. luymesi in the Gulf of Mexico; MacAvoy et al., 2005). This enrichment relative to other cohabiting chemosymbiotic fauna (e.g. vesicomyids) is likely a consequence of metabolic and morphological differences. Symbionts in the two groups use different forms of ribulosebiphosphate carboxylase–oxygenase, which fractionate carbon to different extents (Fisher et al., 1990). It has also been suggested that the different groups take up dissolved inorganic carbon (DIC) that is quite dissimilar in carbon isotopic signature. Although bivalves take up DIC at the sediment surface, which is low in 13C, tubeworms grow with their plumes well above the sediment and hence are able to take up DIC with signatures more typical of seawater (MacAvoy et al., 2005). The similarity between 13C signatures of Lamellibrachia sp. and other photosynthetic food sources (Figure 4) make it difficult to discriminate whether heterotrophs also consume Lamellibrachia. However, siboglinids (e.g. L. luymesi) seem to be unpalatable for predators, probably because they contain chemical compounds that deter consumption (Kicklighter et al., 2004).

The general distribution of stable isotope signatures of the fauna at both the CMSA and control site indicates that primary organic food sources are the same, and mainly of photosynthetic origin (e.g. phytodetritus and SOM). Because the CMSA is located beneath highly productive waters, photosynthetically originated C is expected not to be a limiting factor even at such depths, overriding the potential significance of other locally fixed carbon sources for heterotrophic consumers. However, it is interesting that δ13C values of top predators such as A. rostrata (−17.4 ± 0.1‰), Benthoctopus sp. (−18.9 ± 1.5‰), and even D. eleginoides (−18.6 ± 2.2‰) are more depleted than their expected prey (i.e. background fauna δ13C = –14.3 ± 1.3‰ on average), suggesting partial or occasional inputs from lighter sources (Figure 4). However, although high 15N values for D. eleginoides and Benthoctopus sp. do not really support chemosynthetic food sources, lighter values of A. rostrata at the seep site (Appendix) suggest that this species at least could ingest some chemosynthetic production.

Mechanisms promoting faunal aggregation at the CMSA

Levin and Michener (2002) hypothesized that as food becomes limiting, seep-related resources should comprise a larger part of the diet of non-seep vagrants. For example, at the Oregon margin seeps, also located beneath a highly productive eastern boundary system, the isotopic signatures of mobile sea urchins and crabs closely resemble non-seep production, whereas there is significant incorporation of chemosynthetic material into the benthic foodweb from methane-based communities underlying the oligotrophic waters of the Gulf of Mexico (Levin and Michener, 2002; MacAvoy et al., 2003). At the CMSA, large predatory fish are frequent, and this site seems to be a preferred fishing ground. This is evidenced by abundant lost fishing gear (hooks and weights) in many of the trawls which collected living chemosymbiotic fauna (Sellanes and Krylova, 2005). However, the overall increase in abundance, biomass, and diversity of the megafaunal communities, including those top predators, is not a function of increased local primary production, because there is no reliance on in situ production. Instead, we suggest that the presence of methane-derived authigenic carbonates provides a suitable habitat for sessile organisms and associated fauna. This hard substratum may provide a rich feeding ground for species such as D. eleginoides, because much of their prey (e.g. rattails, cephalopods, and crustaceans; Oyarzún et al., 2001) are present in large quantities there. This has been suggested for the Gorda Escarpment off northern California, where multispecies aggregations of octopus (Benthoctopus sp. and Graneledone sp.) and blob sculpins (Psychrolutes phrictus) brood at seep sites. This preference has been ascribed to the interaction of local topography, physical, and geological settings (Drazen et al., 2003). Females of a local species of blob sculpin (Psychrolutes sio), in an advanced reproductive stage, have been also caught at the CMSA (Table 2), suggesting similar behaviour to their NE Pacific counterparts.

The Chilean margin seep environments seem to act as nuclei for increased diversity and abundance for invertebrates and fish, including commercial species. Damage to these environments by anthropogenic activities may affect the populations of associated species, some of which have been found exclusively at this site, at least up to now. Future studies should describe the extent of seeps across and along the Chilean margin to clarify the species associations and interactions within them and the surrounding non-seep environment, including nearby OMZ. In addition, further studies to elucidate patterns of energy transfer within the system need to include unresolved constituents of the foodweb such as mat-forming bacteria, infauna, and fish. The whole information should facilitate better comparison with other seep settings along the Pacific margin and contribute to improve our understanding of endemicity, biogeographic, bathymetric, and latitudinal zonation patterns of these particular systems.

Acknowledgements

We thank the captain and crew of the Chilean Navy’s RV “Vidal Gormáz” for support at sea, and R. Coffin and J. Díaz-Naveas, who acted as co-chief scientists in the first expedition (VG-04 cruise). Special thanks for help during SeepOx cruise go to V. A. Gallardo, G. Guzmán, L. Dezileau, W. Alarcón, L. Cárdenas, S. Fuentes, J. González, J. Inostroza, P. Inostroza, L. Muñoz, J. Maturana, and M. Silva. Elena Krylova is acknowledged for her help with the taxonomy of vesicomyids, and we are also grateful to L. A. Levin and A. Thurber (Scripps Institution of Oceanography), D. Desbruyères (IFREMER), and two anonymous referees for providing valuable comments on earlier versions of the manuscript. The work was funded by FONDECYT project No. 1061217 to JS, the Research Direction of the University of Concepción and the Centre of Oceanographic Research in the Eastern-South Pacific (COPAS) of the University of Concepción. Additional support was provided by FONDECYT project No. 1061214 to Práxedes Muñoz, Scripps Institution of Oceanography through NOAA Ocean Exploration program Grant # NOAA NA17RJ1231 to L. A. Levin (for ship’s time and cruise participation of CN and J. González).

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Appendix

Carbon and nitrogen stable isotope composition of selected CMSA and control site invertebrates, sedimentary organic matter (SOM), and bottom-water suspended particulate organic material (POM). Samples ordered from higher to lower δ15N, as a relative indicator of trophic position.

Seep site taxa and parameters δ15N (‰)
 
δ13C (‰)
 
n 
 Mean s.d. Mean s.d.  
Psychrolutes sio 23.5 0.8 −14.5 0.4 
Dissostichus eleginoides (>85 cm) 22.1 1.1 −18.6 2.2 
Centroscyllium granulatum 21.8  −14.7  
Coelorinchus fasciatus 21.8  −14.8  
Coryphaenoides ariommus 21.2 1.0 −15.7 0.7 
Stegophiura sp. 20.7  −15.0  
Calliostoma chilena 20.6 1.1 −15.0 0.6 
Miomelon philippiana 20.3  −13.9  
Coralliomorphus sp. 19.9  −18.5  
Munidopsis trifida 19.4 0.3 −15.4 0.2 
Homalopoma panamense 19.3 0.2 −14.3 0.7 
Hyalinoecia sp. 19.1 0.5 −14.8 0.7 
Astrodia tenuispina 18.9  −15.5  
Asteronyx loveni 18.8  −13.5  
Ctenodiscus australis 18.7 2.0 −11.0 1.1 
Bathybembix macdonaldi 18.7 0.4 −14.6 0.2 
Campylonotus semistriatus 18.3 0.2 −14.0 0.3 
Haliporoides diomedeae 18.2 0.4 −15.1 0.3 
Benthoctopus sp. 18.1 2.7 −17.8 1.6 
Limopsis sp. 17.8 0.2 −15.2 0.3 
Aforia cf. goniodes 17.4 0.4 −13.6 0.1 
Callogorgia sp. 16.5  −19.4  
Paragorgia sp. 16.5  −19.7  
Gorgonocephalus chilensis 16.1 2.3 −14.5 1.4 
Turridae 16.0  −14.3  
Ophiura carinata 15.3 1.4 −18.1  
Antimora rostrata 15.0 0.8 −17.4 0.1 
Ophiomusium biporicum 12.6  −17.0  
Thyasira methanophila 10.2  −35.4  
POM 9.8 1.1 −23.5 0.0 
SOM 8.8  −20.18  
Lamellibrachia sp. 7.6  −22.8  
Calyptogena gallardoi 4.8 0.8 −36.4 0.6 
Vesicomyidae gen. sp. 1 2.9 3.7 −36.2 1.3 
Control site taxa and parameters      
Bathyraja sp. 21.9  −14.9  
Bathybembix macdonaldi 21.4  −14.5  
Halaelurus canescens 21.4  −15.2  
Coelorinchus fasciatus 21.3 0.6 −14.8 0.2 
Antimora rostrata 20.1  −16.0  
Fissidentalium majorinum 19.4  −17.2  
Stereomastis sculpta 19.3  −16.8  
Haliporoides diomedea 19.1  −15.1  
Puncturella sp. 18.1  −14.3  
+Benthoctopus sp. 18.0  −16.9  
Ennucula grayi 15.1  −15.7  
Macrocystis sp. debris 12.0  −14.2  
SOM 8.0  −20.1  
Seep site taxa and parameters δ15N (‰)
 
δ13C (‰)
 
n 
 Mean s.d. Mean s.d.  
Psychrolutes sio 23.5 0.8 −14.5 0.4 
Dissostichus eleginoides (>85 cm) 22.1 1.1 −18.6 2.2 
Centroscyllium granulatum 21.8  −14.7  
Coelorinchus fasciatus 21.8  −14.8  
Coryphaenoides ariommus 21.2 1.0 −15.7 0.7 
Stegophiura sp. 20.7  −15.0  
Calliostoma chilena 20.6 1.1 −15.0 0.6 
Miomelon philippiana 20.3  −13.9  
Coralliomorphus sp. 19.9  −18.5  
Munidopsis trifida 19.4 0.3 −15.4 0.2 
Homalopoma panamense 19.3 0.2 −14.3 0.7 
Hyalinoecia sp. 19.1 0.5 −14.8 0.7 
Astrodia tenuispina 18.9  −15.5  
Asteronyx loveni 18.8  −13.5  
Ctenodiscus australis 18.7 2.0 −11.0 1.1 
Bathybembix macdonaldi 18.7 0.4 −14.6 0.2 
Campylonotus semistriatus 18.3 0.2 −14.0 0.3 
Haliporoides diomedeae 18.2 0.4 −15.1 0.3 
Benthoctopus sp. 18.1 2.7 −17.8 1.6 
Limopsis sp. 17.8 0.2 −15.2 0.3 
Aforia cf. goniodes 17.4 0.4 −13.6 0.1 
Callogorgia sp. 16.5  −19.4  
Paragorgia sp. 16.5  −19.7  
Gorgonocephalus chilensis 16.1 2.3 −14.5 1.4 
Turridae 16.0  −14.3  
Ophiura carinata 15.3 1.4 −18.1  
Antimora rostrata 15.0 0.8 −17.4 0.1 
Ophiomusium biporicum 12.6  −17.0  
Thyasira methanophila 10.2  −35.4  
POM 9.8 1.1 −23.5 0.0 
SOM 8.8  −20.18  
Lamellibrachia sp. 7.6  −22.8  
Calyptogena gallardoi 4.8 0.8 −36.4 0.6 
Vesicomyidae gen. sp. 1 2.9 3.7 −36.2 1.3 
Control site taxa and parameters      
Bathyraja sp. 21.9  −14.9  
Bathybembix macdonaldi 21.4  −14.5  
Halaelurus canescens 21.4  −15.2  
Coelorinchus fasciatus 21.3 0.6 −14.8 0.2 
Antimora rostrata 20.1  −16.0  
Fissidentalium majorinum 19.4  −17.2  
Stereomastis sculpta 19.3  −16.8  
Haliporoides diomedea 19.1  −15.1  
Puncturella sp. 18.1  −14.3  
+Benthoctopus sp. 18.0  −16.9  
Ennucula grayi 15.1  −15.7  
Macrocystis sp. debris 12.0  −14.2  
SOM 8.0  −20.1  

s.d., standard deviation; n, number.