Abstract
The sighting of giant bivalves and tubeworms at the Rose Garden vent field on the Galápagos Rift in 1977 marked the discovery of hydrothermal vents, a turning point for modern biology. The following decade saw a flurry of taxonomic descriptions of vent endemic species from the first vents. With the finding of high-temperature ‘black smokers’ on the East Pacific Rise, exploration shifted away from Galápagos. A faunal list of Galápagos vents with 65 species was published in 1991, then updated to 74 species in 2006. Since then, few expeditions revisited the Galápagos Rift. Here, we revisited several Galápagos vents including recently confirmed high-temperature sites and inactive sulfide mounds. From our collecting efforts and observations, we update the faunal list to 88 species including 15 new records, restricted to obvious vent associates. Accurate regional faunal lists are important for understanding the biogeography of vent fauna, and our list will also be valuable for setting management strategies.
Introduction
The discovery of hydrothermal vents themselves on the eastern Galápagos Rift in 1977 was not really a surprise, as geologists had predicted their presence from the missing heat measured near ridge axes (Sclater and Klitgord 1973) and warm buoyant plumes collected by a towed vehicle (Weiss et al. 1977). But nobody was prepared for the first contact with its bizarre inhabitants at a supposedly nutrient-deficient deep seabed two and a half kilometres below the surface – dense aggregations of giant clams and mussels, worms living in metre-long white tubes with red plumes swaying in shimmering water, and all other animals living with them (Corliss et al. 1979). Starting with the description of the giant vent clam Turneroconcha magnifica and the bythograeid vent crab Bythograea thermydron (Boss and Turner 1980; Williams 1980) followed by the giant tubeworm Riftia pachyptila and the discovery of chemosymbiosis (Cavanaugh et al. 1981; Jones 1981), biologists began to tease apart the taxonomic affinities and evolutionary origins of these creatures (Hessler and Smithey 1983).
Within a decade of its discovery, nearly all animals found in the original diffuse flow Galápagos Rift vents, now known as the Rose Garden vent field, were described. An early faunal list in 1991 included 65 species (Tunnicliffe 1991; Tunnicliffe 1992), and another in 2006 listed 74 (Desbruyères et al. 2006). With the discovery of ‘black smoker’ chimneys spewing out high-temperature fluids in other systems such as East Pacific Rise (EPR) and Juan de Fuca Ridge (Tunnicliffe et al. 1985; Desbruyères and Laubier 1986), exploration shifted away from Galápagos Rift where vigorous venting was apparently lacking. An expedition in 2002 found Rose Garden had been buried under fresh basaltic lava flows and the communities had been largely wiped out except some recent settlers on nearby low-temperature venting from cracks in an area named Rosebud (Shank et al. 2003). The 2002 expedition also found signals for more vents east of Rose Garden on the eastern rift, plus a vent at the western Galápagos Rift near the Galápagos Islands. Between 2005-2006, towed-camera surveys in the western Galápagos Rift confirmed the first high-temperature chimneys (Haymon et al. 2008). Though these sites provide likely grounds for new records and subsequent research cruises have visited some of these areas using underwater vehicles (Shank et al. 2012; Raineault et al. 2016), no faunal updates have been published to date.
From October to November 2023, we were able to revisit the Galápagos Rift vents on-board the Schmidt Ocean Institute’s R/V Falkor (too) during the research cruise FKt231024. The cruise aimed to 1) use high-resolution acoustic mapping (remotely-operated vehicle based multibeam and interferometric synthetic aperture sonar) to generate detailed geological and habitat maps of hydrothermal vents along parts of the Eastern and Western Galápagos Spreading Centres; and 2) investigate the distributions of animal communities associated with both active and inactive vents. Here, we revise the faunal list of Galápagos Rift hydrothermal vents based on the literature since the last compilation (Desbruyères et al. 2006) plus new findings from our research expedition, in order to present all reliable distribution records from vents in this region.
Materials and Methods
During R/V Falkor (too) cruise Fkt231024, we visited several hydrothermal vent fields on the Galápagos Rift using the remotely operated vehicle (ROV) SuBastian. These included Rose Garden / Rosebud (0.81°N, 86.22°W, 2450-2550 m deep; dive #603) and Tempus Fugit (0.77°N, 85.91-93°W, 2500-2560 m; dive #606-607, 609) on the eastern Galápagos Rift (Shank et al. 2012; Raineault et al. 2016); as well as Iguanas-Pinguinos (2.10°N, 91.89-94°W, 1650-1700 m; dive #611-613) and Tortugas, a newly-discovered active vent field on the western edge of the East Los Huellos Caldera (0.95°N, 90.53-56°W, 1500-1600 m; dive #614) on the western Galápagos Rift (Haymon et al. 2008). An overview map of the study area is presented in Figure 1.
Map of the study area, showing the location of each hydrothermal vent field visited during R/V Falkor (too) research cruise Fkt231024.
We used video and screengrabs from a 4K ultra-HD video camera (SULIS Subsea Z70; resolution 3840 x 2160 pixels) on the ROV SuBastian for seafloor imaging, which allowed up to 12x zoom for close-up observations of even smaller animals. Animals were collected using either a seven-function manipulator arm (Schilling Robotics TITAN 4) or a suction sampler mounted on ROV SuBastian. Upon recovery on-board, animals were sorted in cold (4°C) seawater, cleaned with a brush, and photographed using a Canon EOS 5Ds R digital single-lens reflex camera equipped with a Canon EF 100 mm F2.8L MACRO IS USM macro lens. Most new records are based on collected specimens, but some larger fauna were identified using close-up imagery.
Previously published faunal lists for the Galápagos Rift vents (Tunnicliffe 1991; Tunnicliffe 1992; Desbruyères et al. 2006) were examined for taxonomic status using both the World Register of Marine Species (WoRMS Editorial Board 2023) and primary literature. We aimed to remove erroneous records and to ensure the list only includes those species that rely strongly on the vent environment. To eliminate erroneous records, occurrence records at the Galápagos Rift were checked against the original descriptions and subsequent works on each species; geographic distribution of those species found in other hydrothermal systems were also recorded (see Table 1). New species described since the publication of the previous lists were checked in Google Scholar using search terms “Galapagos AND hydrothermal AND new species”. New records from our present study are added to this list.
Species newly recorded in this study are listed in bold, species records from imagery only are denoted with asterisks. Abbreviations: GAL = Galápagos Rift; EPR = East Pacific Rise; GMS = Guaymas Basin; MBC = Monterey Bay, California. “?” in distribution means occurrence outside Galápagos Rift remains uncertain.
Results and Discussion
Overview of vent fields visited
In the eastern Galápagos Rift, the Rose Garden / Rosebud area was covered by fresh basaltic lava flow and devoid of living vent fauna. This confirms the finding from a 2011 cruise that another eruption event between 2005 and 2011 had eliminated fauna in this field (Shank et al. 2012). Furthermore, we revisited a serpulid worm colony found in 2015 (Raineault et al. 2016) in case living vent fauna persisted (0.8049°N, 86.2194°W, 2447 m deep), but only found decaying serpulid tubes and dissolving mussel shell debris. As such, venting at Rose Garden has likely ceased – although we did not visit the location of the East of Eden field. In the nearby Tempus Fugit field (Raineault et al. 2016), we found that venting at the previously known main diffuse flow site (0.7700°N, 85.9114°W, 2561 m deep) had waned, with few living vesicomyid clams and Riftia tubeworms. Nevertheless, we found a new diffuse flow vent nearby (0.7712°N, 85.9236°W, 2602 m deep; ‘Walking Dead’ vent). We also revisited the active chimney (Raineault et al. 2016) at the western end of Tempus Fugit (0.7712°N, 85.9332°W, 2514 m deep; ‘Zombie’ vent) and confirmed high-temperature (>200°C; measured with the ROV temperature probe) venting there. A number of dead spires or inactive mounds were found around the Zombie vent and were also surveyed.
Shifting to the western Galápagos Rift, we revisited all three vent sites in the Iguanas-Pinguinos vent field (Haymon et al. 2008; Raineault et al. 2016), including Iguanas West (2.0992°N, 91.9053°W, 1670 m), Iguanas East (2.1050°N, 91.9378°W, 1670 m), and Pinguinos (2.0993°N, 91.9052°W, 1670 m). We confirmed chimney structures associated with vigorous venting of high-temperature fluid at all three locations. At East Los Huellos Caldera, where only plume signals were known (Haymon et al. 2008), we discovered active venting associated with chemosynthetic communities. This included both diffuse venting areas dominated by mussels and vesicomyid clams (0.9546°N, 90.5566°W, 1590 m) and active chimney complexes with high-temperature (>250°C) venting (0.9543°N, 90.5613°W, 1520 m).
Revising the existing faunal list
The most recent faunal list of the Galápagos Rift vents (Desbruyères et al. 2006) included a total of 74 species. Of these, two orbiniid annelid species including Orbiniella aciculata and Scoloplos ehlersi were erroneously included in the list, as the author clearly states these were collected from box cores deployed near the Galápagos Rift but were not from the vent community (Blake 1985). Here, we further remove the lysianassoid amphipod Abyssorchomene abyssorum on the grounds that it is a globally distributed deep-sea species found in non-chemosynthetic seafloor and that its vent record is based on a single specimen that may have been a by-catch (Barnard and Ingram 1990). Similarly, we took out the abyssal grenadier Coryphaenoides armatus since it is merely an occasional visitor to vents from the surrounding deep sea. Though there are two species of dubious taxonomic status – the hesionid polychaete Nereimyra alvinae with poorly preserved types (Pleijel et al. 2012) and the crab Bythograea intermedia described from megalopa and juveniles only (de Saint Laurent 1988) – we have kept them, pending future taxonomic revision. The melanodrymid snail Melanodrymia sp. and the raphitomid snail Nepotilla sp. were initially reported in a conference abstract (Gustafson 1991) and then included in a gastropod faunal list by taxonomic experts (Warén and Bouchet 1993). Though their species-level identification remains unclear, they remain on the list pending more taxonomic information.
Since the 2006 list was published, two additional species have been recorded from Galápagos Rift in the published literature. The first is the Pompeii worm Alvinella pompejana, visually confirmed from Tempus Fugit vent field in 2010, but not sampled (Raineault et al. 2016). The second is Lepetodrilus aff. tevnianus Galápagos sensu Matabos and Jollivet (2019), morphologically resembling Lepetodrilus tevnianus found on the EPR vents but is a genetically distinct lineage considered to represent an undescribed species (Matabos and Jollivet 2019). Altogether, these bring the historical species occurrence record to 72 species.
New records
From our observations and collecting efforts during the 2023 cruise, we encountered a total of 15 species that are clearly associated with the chemosynthetic ecosystem and not previously recorded from Galápagos Rift vents (Tunnicliffe 1992; Desbruyères et al. 2006). Table 1 lists our updated full faunal list with our new records shown in bold. Figure 2 presents key in situ screengrabs including records based on species clearly identifiable from imagery, while figure 3 shows photographs of specimens collected. In the following paragraphs, we provide more details on our newly recorded species.
In situ imagery of Galápagos Rift vents captured by screengrabs of the 4K video camera in the present study: a the alvinellid worm Alvinella caudata on chimney wall of Zombie vent, Tempus Fugit; b two individuals of the bythograeid crab Cyanagraea praedator, Zombie vent, Tempus Fugit; c a living individual of Nodopelta rigneae (white arrow), Zombie vent, Tempus Fugit; d Lebbeus laurentae (larger shrimp on the right) seen with Alvinocaris lusca at the base of the active chimney complex at West Iguanas, Iguanas-Pinguinos; e a bouquet of Tevnia jerichonana tubeworms at a peripheral diffuse flow at West Iguanas, Iguanas-Pinguinos; f a cluster of Oasisia alvinae tubeworms at a diffuse flow site in East Los Huellos Caldera and several individuals of Sericosura pycnogonids nearby (white arrow); g several hydrozoan Candelabrum cf. phrygium near a low-temperature vent at West Iguanas, Iguanas-Pinguinos; h two individuals of the true limpet Neolepetopsis densata on inactive chimneys near Zombie vent, Tempus Fugit.
Specimens collected from Galápagos Rift vents in the present study. a Phymorhynchus major, Walking Dead diffuse flow vent, Tempus Fugit; b Peltospira sp., Zombie vent, Tempus Fugit; c Neolepetopsis densata, inactive spires near Zombie vent, Tempus Fugit; d Nodopelta rigneae, Zombie vent, Tempus Fugit; e young individual of Peltospira delicata, Zombie vent, Tempus Fugit; f Candelabrum cf. phrygium, West Iguanas, Iguanas-Pinguinos; g a juvenile individual of Tevnia jerichonana from Zombie vent, Tempus Fugit; h Sericosura sp., diffuse flow at East Los Huellos Caldera; i Sericosura cyrtoma, diffuse flow at East Los Huellos Caldera; j Hesiolyra bergi, Zombie vent, Tempus Fugit; k Alvinella caudata, Zombie vent, Tempus Fugit; l Alvinella pompejana, Zombie vent, Tempus Fugit.
The alvinellid worm Alvinella caudata (Fig. 2a, 3k) was seen on active chimney walls at Tempus Fugit, Iguanas-Penguinos, and Tortugas. It co-occurred with A. pompejana, and both were collected together at Tempus Fugit; we show a specimen photo of A. pompejana (Fig. 3l) since this is the first time a specimen was collected from Galápagos Rift and serves as a confirmation of the previous record (Raineault et al. 2016). Also found on the same habitat was the hesionid worm Hesiolyra bergi (Fig. 3j) which occurred in aggregations on the chimneys and were sometimes seen going into tubes of Alvinella worms. The bythograeid crab Cyanagraea praedator (Fig. 2b) was common on the active chimneys too, readily identified from images by the well-developed eye-stalk sockets and their large size (de Saint Laurent 1984). The association between Cyanagraea and Alvinella is also known from EPR vents, where the former is a predator of the latter (Desbruyères et al. 2006).
We also collected three species of peltospirid gastropods from the high-temperature Zombie vent at Tempus Fugit, including Nodopelta rigneae (Fig. 3d), Peltospira delicata (Fig. 3e), and a likely undescribed species of Peltospira (Fig. 3b). Although only one damaged specimen of N. rigneae could be collected, several individuals were seen near Alvinella tubes (Fig. 2c). Peltospira delicata is also recorded based on a single specimen; though it is a juvenile still with operculum attached, the characteristic shell sculpture is clearly displayed (McLean 1989a). The likely undescribed Peltospira species, recorded based on two collected specimens, lacks clear spiral ridges on the body whorl. This feature is shared with Peltospira operculata, but, unlike P. operculata (McLean 1989a; Warén and Bouchet 2001), in our species the spiral sculpture is lacking even in the early whorls, the coiling is weaker, and the operculum is lacking in adults. Peltospirid snails were not seen on active chimneys in the western Galápagos Rift, but as we did not sample those sites, we may have missed them on video due to their small size.
At both diffuse flow areas and active chimney walls in Iguanas-Pinguinos and Tortugas we saw bouquets of the tubeworm Tevnia jerichonana (Fig. 2e), and a single juvenile specimen (Fig. 3g) was collected from the Zombie vent at Tempus Fugit where no adults could be seen. Only at the diffuse flow site at Tortugas, did we see a cluster of Oasisia alvinae. The only tubeworm known from previous explorations in the eastern Galápagos Rift was Riftia pachyptila (Corliss et al. 1979; Jones 1981; Raineault et al. 2016), which also occurred in both diffuse flow sites in Tempus Fugit (but in lower abundance than previous expeditions due to waning activity there). Conversely, at the western Galápagos Rift we did not see any sign of Riftia. At Tortugas, we found two species of the pycnogonid genus Sericosura in abundance around diffuse flows (Fig. 2f). One species with seven-segmented palps was readily identifiable as Sericosura cyrtoma (Fig. 2h), but the other (Fig. 2i) with nine-segmented palps did not match any described eastern Pacific congeners (Child 1987; Child and Segonzac 1996; Wang et al. 2013) and may represent an undescribed species. Though we did not find pycnogonids in the eastern Galápagos Rift, a previous cruise reported seeing pycnogonids there (Raineault et al. 2016), likely also Sericosura.
The raphitomid snail Phymorhynchus was often seen in the periphery zone of all vent fields we visited. Initially, Phymorhynchus from the Galápagos Rift was considered to be conspecific with those on the EPR (Warén and Bouchet 1989), but this distribution record was not mentioned when P. major was formally named based on only EPR material (Warén and Bouchet 2001). Here, we collected a specimen (Fig. 3a) and confirm the presence of P. major in the Galápagos. Though not seen on our expedition, we note that a recent expedition also on R/V Falkor (too) (Fkt230812) encountered dense coverage of a vent barnacle tentatively identified as Eochionelasmus cf. paquensis (Hiromi K. Watanabe, pers. comm.) at a vent site named Sendero del Cangrejo (2.53°N, 94.33°W, 2490 m deep). This species is added to our list based on imagery shown on an openly available YouTube stream of ROV SuBastian dive #573 at this site (Schmidt Ocean Institute 2023).
We also saw several individuals of Lebbeus laurentae (Komai et al. 2012) co-occurring with Alvinocaris lusca on the vent periphery only in the West Iguanas vent (Fig. 2d). Numerous individuals of the hydrozoan Candelabrum were seen also near the periphery of West Iguanas (Fig. 2g). The collected individual (Fig. 3f) was morphologically similar to Candelabrum phrygium which has a pan-arctic distribution and also known from Mid-Atlantic Ridge vents (Segonzac and Vervoort 1995). As Galápagos is far from its known range, we consider it likely to be a distinct species and tentatively identified it as C. cf. phrygium. Further away from high-temperature venting, we found many individuals of the true limpet Neolepetopsis densata on inactive chimneys near Zombie vent near Tempus Fugit (Fig. 2h, 3c). This species was likely missed by earlier cruises due to Neolepetopsis being a genus apparently restricted to inactive vents (McLean 1990; Chen et al. 2021).
During our exploration we also saw a number of animals typical of non-chemosynthetic seafloor environments within proximity to vents, such as the Pacific white skate Bathyraja spinosissima known to incubate egg cases at Galápagos Rift vents (Salinas-de-León et al. 2018), the octopus Graneledone (likely an undescribed species, Janet Voight pers. comm.) (Desbruyères et al. 2006), and some encrusting demosponges. We did not include them in our list due to the likely incidental nature of their presence in or near the chemosynthetic ecosystem.
Conclusions
We revised the existing faunal list of Galápagos Rift vents and added 15 new records based on our observations and specimens collected, bringing the total to 88 species. Of these, at least 15 species are only known from Galápagos Rift vents (Table 1), an endemism rate of 17%. Though only based on qualitative observations, our results suggest some differences in fauna composition of vents at eastern vs western Galápagos Rift, warranting future research. Accurate species lists and occurrence data can reveal key processes driving the biogeographic patterns and evolution of hydrothermal vent fauna in general (Giguère and Tunnicliffe 2021; Brunner et al. 2022). Such data provide important grounds for constructing management strategies and spatial planning, especially with the growing interests for deep-sea mineral resources. As the Galápagos Rift is partially included in the Galápagos Marine Reserve, our updated species list will also be useful for conservation and marine spatial planning in this world heritage site.
Funding
The research cruise FKt231024 on-board R/V Falkor (too) was funded by the Schmidt Ocean Institute.
Author Contributions
CC and VT conceived the project. CC and VT identified animal species, and updated the faunal list. CC undertook photography and made the figures. JWJ secured funding, planned and led the expedition, provided map of the research area. CC drafted the original manuscript which was critically revised by JWJ and VT. All authors agreed to the submission of the final version.
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
Study species were invertebrates and no experimental manipulation was undertaken on live animals in this study. All necessary permits for sampling and observation have been obtained by the authors where applicable. Permission for ROV dives inside the Galápagos Marine Reserve in Ecuador was granted through a partnership between Schmidt Ocean Institute and the Charles Darwin Foundation (MAATE-DPNG/DGA-2023-1449-O).
Data availability
Data relevant to our conclusions are included in the main text. Specimens collected within the Galápagos Marine Reserve are vouchered in the Charles Darwin Research Station on Santa Cruz Island (https://www.darwinfoundation.org/en/about/cdrs). All ROV SuBastian dives during cruise FKt231024 are available online through the Schmidt Ocean Institute YouTube page: https://www.youtube.com/@SchmidtOcean/streams
Acknowledgements
We thank the captain and crew of R/V Falkor (too) during the research cruise Fkt231024 (‘Project Zombie: Bringing dead vents to life – Ultra fine-scale seafloor mapping’), as well as the ROV SuBastian team for their immense support. To clarify, (We Were Never Promised A) Rose Garden on this cruise. Viola Watts (University of Victoria), Janet Voight (The Field Museum), Hiromi K. Watanabe (JAMSTEC), and Anders Warén (Swedish Museum of Natural History) are thanked for helping with identifications and historical records. Ana-Belén Yánez Suárez (Marine Institute of Memorial University of Newfoundland) and Stuart Banks (Charles Darwin Research Station) are gratefully acknowledged for facilitating permissions to carry out research within the Galápagos Marine Reserve in Ecuador. The cruise FKt231024 was supported and authorised by the Galápagos National Park Directorate, the Instituto Oceanográfico y Antártico de la Armada de Ecuador (INOCAR) and facilitated by the Charles Darwin Foundation Deep-Ocean Research Program under permit number PC 51-23. This publication is contribution number 2602 of the Charles Darwin Foundation for the Galápagos Islands. We also thank our on-board Ecuadorian observers, Diego Bermeo (Galápagos National Park) and Richard Porfirio Narea Ortega (INOCAR). We recognize the extensive support from the Schmidt Ocean Institute for this expedition and associated logistics.