Differences in recovery between deep-sea hydrothermal vent and vent-proximate communities after a volcanic eruption

https://doi.org/10.1016/j.dsr.2015.10.008Get rights and content

Highlights

  • A volcanic eruption destroyed communities at the East Pacific Rise, 9°50′N in 2006.

  • Recovery patterns and dispersal of benthic communities were analyzed over 4 years.

  • About 40% of original meio- and macrofaunal species returned after 4 years at vents.

  • Only 28% of meio- but 67% of macrofaunal species had come back to basalt areas.

  • Both, vent and basalt habitats need conservation efforts regarding deep-sea mining.

Abstract

Deep-sea hydrothermal vents and the surrounding basalt seafloor are subject to major natural disturbance events such as volcanic eruptions. In the near future, anthropogenic disturbance in the form of deep-sea mining could also significantly affect the faunal communities of hydrothermal vents. In this study, we monitor and compare the recovery of insular, highly productive vent communities and vent-proximate basalt communities following a volcanic eruption that destroyed almost all existing communities at the East Pacific Rise, 9°50′N in 2006. To study the recovery patterns of the benthic communities, we placed settlement substrates at vent sites and their proximate basalt areas and measured the prokaryotic abundance and compared the meio- and macrofaunal species richness and composition at one, two and four years after the eruption. In addition, we collected samples from the overlying water column with a pelagic pump, at one and two years after the volcanic eruption, to determine the abundance of potential meiofauna colonisers. One year after eruption, mean meio- and macrofaunal abundances were not significantly different from pre-eruption values in vent habitats (meio: 8–1838 ind. 64 cm−2 in 2006; 3–6246 ind. 64 cm−2 in 2001/02; macro: 95–1600 ind. 64 cm−2 in 2006; 205–4577 ind. 64 cm−2 in 2001/02) and on non-vent basalt habitats (meio: 10–1922 ind. 64 cm−2 in 2006; 8–328 ind. 64 cm−2 in 2003/04; macro: 14–3351 ind. 64 cm−2 in 2006; 2–63 ind. 64 cm−2 in 2003/04), but species recovery patterns differed between the two habitat types. In the vent habitat, the initial community recovery was relatively quick but incomplete four years after eruption, which may be due to the good dispersal capabilities of vent endemic macrofauna and vent endemic dirivultid copepods. At vents, 42% of the pre-eruption meio- and 39% of macrofaunal species had returned. In addition, some new species not evident prior to the eruption were found. At the tubeworm site Tica, a total of 26 meio- and 19 macrofaunal species were found in 2009, which contrasts with the 24 meio- and 29 macrofauna species detected at the site in 2001/02. In the basalt habitat, community recovery of meiofauna was slower with only 28% of the original 64 species present four years after eruption. The more limited dispersal capabilities of meiofauna basalt specialists such as nematodes or harpacticoid copepods probably caused this pattern. In contrast, 67% of the original 27 macrofaunal species had recolonized the basalt by 2009. Our results suggest that not only vent communities, but also species-rich communities of vent-proximate habitats require attention in conservation efforts.

Introduction

All organisms living at deep-sea hydrothermal vents and on vent-proximate basalt are subject to natural disturbances, i.e. volcanic eruptions. On fast spreading ridges like the 9°50′N East Pacific Rise (EPR), eruptions occur frequently, with time intervals of only 15 years, and vent sites are typically separated by a few kilometers (Haymon et al., 1991, Shank et al., 1998, Tolstoy et al., 2006). In contrast, vent sites on slow spreading centers are more distant from each other and major disturbance events occur less frequently (German et al., 1996, Humphris et al., 2002, Murton et al., 1994). Organisms occur in a wide range of environmental conditions, and it is crucial to consider dispersal and connectivity patterns of meio- and macrofauna in order to address recovery mechanisms in response to disturbance and productivity regimes. Vent animals live in highly dynamic environments, with intermittent exposure to temperature peaks, substantial concentrations of hydrogen sulfide, variable heavy metal exposure, and reduced oxygen availability, but high in situ primary production. Megafauna, such as tubeworms or mussels, act as foundation species and provide a habitat for the associated macro- and meiofauna (Fisher et al., 2007, Van Dover, 2000). The endemism, abundance, and biomass of vent macrofaunal communities is much higher, but diversity is much lower than sedimented deep-sea habitats at similar depths (Moalic et al., 2012, Tunnicliffe, 1992). Macrofaunal dispersal between isolated vent sites occurs primarily in the larval stage, but demersal, dispersal and migration can also occur (Mullineaux et al., 2010, Mullineaux et al., 2005). In general, meiofauna are similarly diverse to macrofauna, but are not exceptionally abundant, and many vent meiofaunal species are not restricted to vents, but also occur on proximate basalt (Gollner et al., 2010b, Gollner et al., 2007). The dispersal mechanisms of vent meiofauna have not been studied yet.

On basaltic rock proximate to vents under ambient deep-sea conditions, low temperatures are stable and in situ primary production is negligible. The source of nutrition is suspended photosynthetic-derived material from surface waters and particulate organic matter originating from the nearby active vents (Erickson et al., 2009, Levin et al., 2009). Dominant macrofauna include sparsely distributed sponges, hydroids, anemones, squat lobsters, ophiuroids, and holothurians (Galkin, 1997). In addition, vent-associated macrofaunal taxa were found on proximate basalt, although in low abundance and low biomass (Gollner et al., 2015, Marcus and Tunnicliffe, 2002). At 9°50′N East Pacific Rise, a species-rich but low abundance meiofaunal community was documented on vent-proximate basalt (Gollner et al., 2010b). Dispersal and biogeography of basalt species are almost unknown, but a macrofaunal study showed unexpectedly high levels of genetic differentiation for squat lobsters (Thaler et al., 2014).

The East Pacific Rise, like other mid ocean ridges, has rich deposits of metals in the form of massive sulfide deposits (SMS). Currently, various regions along the Mid Atlantic Ridge and the Indian Ocean Triple Junction are being explored for mining (SPC, 2013). Exploitation of sulfide minerals is expected to disturb communities living at hydrothermal vents and in surrounding areas (Van Dover, 2011). The first deep-sea massive sulfide mine could open in Papua New Guinea as soon as 2016 (Gramling, 2014). However, the scale of environmental impacts remains to be determined, and there are many unknowns in the ecology and connectivity of populations at active and inactive SMS deposits (Boschen et al., 2013, Van Dover, 2011). Recommendations to evaluate the possible impact of mining (disturbance) include identification of conservation areas, as well as determination of natural conservation units for key species with different size and life histories and dispersal strategies (Van Dover, 2011). Different life-histories of meio- and macrofauna include for example mode of development (direct benthic versus planktonik), dispersal (as adults versus as larvae), generation time (less than one year versus more than one year), or potential number of off-spring (small versus large) (Warwick, 1984). Within the meiofauna, nematodes show less dispersal potential than copepods (Giere, 2009). The effect of disturbance on the vent-proximate basalt areas has received relatively less attention than vent habitats, although future mining operations will probably mostly impact the vent-surroundings with their mining-machines. Volcanic eruptions naturally disturb hydrothermal vents and the vent-proximate areas; understanding these recovery mechanisms will help to formulate plans for future conservation.

The recent volcanic eruption at the 9°50′N EPR in 2005/2006 covered an area of several km2 with lava (Tolstoy et al., 2006) (see Fig. 1) and provided the opportunity to examine colonization and recovery patterns of meio- and macrofauna in hydrothermal vent and ambient basalt habitats. In particular, we consider the influence of species-specific traits such as dispersal ability and contrast patchy (active vent) and continuous habitat areas (ambient bare basalt). We hypothesize that vent-restricted species have high dispersal potential and therefore relatively rapid recovery rates after disturbance, whilst species in the continuous non-vent basalt habitat might have less potential to disperse over wider distances and thus could delay recovery. In addition, the general high abundances of single species at vents (e.g. Fisher et al., 2007) could enhance recovery, whilst the general low abundances of standing populations (and thus gametes) of single species on basalt (Gollner et al., 2015, Gollner et al., 2010b) could slow down recovery. Further, we hypothesize that life-history traits of meio- and macrofauna influence recolonization. We infer that macrofauna have high dispersal potential and can quickly colonize the disturbed area. Within the meiofauna we expect that copepods show greater dispersal and thus faster colonization than nematodes. A study on nematode recovery after the eruption at the 9°50′N EPR already showed that nematodes apparently required a relatively long time to colonize the lava-flooded area (vent and basalt) in greater numbers and richness (Gollner et al., 2013).

To study recovery patterns in the benthic community, we placed settlement substrates at recently established vent tubeworm sites and their proximate basalt areas. We examined meio- and macrofaunal abundances, species richness and composition at one, two and four years after the eruption. To study potential food-limitation after eruption (bottom-up control), prokaryote abundances were analyzed one year after eruption at vents and on basalt. Abundances of newly assembled meio- and macrofaunal communities after the eruption were also compared to benthic communities sampled prior to the eruption in 2001–2004 (Gollner et al., 2015, Gollner et al., 2010b). To determine the influence of dispersal on benthic community recovery, macrofaunal larvae (Mullineaux et al., 2010) and meiofauna were collected with pelagic pumps one and two years after eruption.

Section snippets

Benthic collections

To obtain quantitative meio- and macrofaunal species abundances, three settlement substrates each were recovered at the vent sites Tica, Sketchy, and P-Vent, and three settlement substrates on proximate bare basalt areas. They were all located at ~2500 m depth in the 9°50′N region of the East Pacific Rise (EPR) and were studied over four years, in December 2006, November 2007 and December 2009 (Table 1, Fig. 1, Fig. 2). Each settlement substrate used at vent habitats consisted of 2 plastic

Benthic community

Prokaryote abundances were high one year after the eruption, with mean 3.5E+11 64 cm−2 at Tica vent, 2.3E+11 64 cm−2 at P-Vent, 6.2E+10 64 cm−2 at Sketchy vent, and 2.3E+10 64 cm−2 on basalt (Table 1). Prokaryote abundance was significantly lower on basalt than at the vent sites Tica (p=0.003) and P-Vent (p<0.001), but similar to the vent site Sketchy (p=0.07). At vents and on basalt, mean meio- and macrofauna abundances were not statistically discriminable to pre-eruption values within one year

Recovery of abundance

The rather rapid recovery of meio- and macrofauna abundance suggests that the environment is suitable to support a relatively abundant vent and basalt community soon after a major disturbance. About one year after eruption, vent sites had large aggregations of T. jerichonana supporting an abundant associated community. The main characteristics of vent habitats, i.e. temperature, pH and sulfide ranges and their relationships, were not substantially different at our sites to levels measured among

Conclusions and implications for conservation

The dispersal ability of organisms is a key trait to determine metacommunity structure (De Bie et al., 2012) and influences the recovery of vent and basalt habitats after an eruption. While species richness recovery was rather quick but incomplete at hydrothermal vents, slower recovery was observed on basalt. Vent fields are patchily distributed and isolated from each other and recolonization via dispersal of planktonic larvae is vital for the persistence of populations. Hence, the arrival of

Contributions

All authors contributed to writing of the manuscript and approved the final article.

S.G. and M.B. were responsible for project development, analyses of data and writing of the manuscript. S.G. identified meiofauna and macrofauna; B.G. identified macrofauna; P.M.A. identified meiofauna; S.M. performed water column sampling; N.L.B. measured and analysed abiotic variables; M.W. analysed prokaryote abundances; T.M.S. provided 3 month-long deployed benthic control samples.

Conflict of interest

The authors declare that they have no conflict of interest.

Acknowledgments

We received funding from the Austrian FWF (Grant P20190-B17; M. Bright), thGerman Humboldt Foundation post-doc scholarship to S. Gollner), the American NSF (Grant OCE-0424953; L. Mullineaux, A. Thurnherr, J. Ledwell), and the European Union Seventh Framework Programme (FP7/2007-2013) under the MIDAS project, Grant agreement no. 603418. Ifremer and CNRS (France) supported N. Le Bris cruise participation and sensor developments. B. Govenar was supported by a postdoctoral fellowship from the Deep

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