Detecting the Influence of Initial Pioneers on Succession at Deep-Sea Vents

Abstract

Deep-sea hydrothermal vents are subject to major disturbances that alter the physical and chemical environment and eradicate the resident faunal communities. Vent fields are isolated by uninhabitable deep seafloor, so recolonization via dispersal of planktonic larvae is critical for persistence of populations. We monitored colonization near 9°50′N on the East Pacific Rise following a catastrophic eruption in order to address questions of the relative contributions of pioneer colonists and environmental change to variation in species composition, and the role of pioneers at the disturbed site in altering community structure elsewhere in the region. Pioneer colonists included two gastropod species: Ctenopelta porifera, which was new to the vent field, and Lepetodrilus tevnianus, which had been rare before the eruption but persisted in high abundance afterward, delaying and possibly out-competing the ubiquitous pre-eruption congener L. elevatus. A decrease in abundance of C. porifera over time, and the arrival of later species, corresponded to a decrease in vent fluid flow and in the sulfide to temperature ratio. For some species these successional changes were likely due to habitat requirements, but other species persisted (L. tevnianus) or arrived (L. elevatus) in patterns unrelated to their habitat preferences. After two years, disturbed communities had started to resemble pre-eruption ones, but were lower in diversity. When compared to a prior (1991) eruption, the succession of foundation species (tubeworms and mussels) appeared to be delayed, even though habitat chemistry became similar to the pre-eruption state more quickly. Surprisingly, a nearby community that had not been disturbed by the eruption was invaded by the pioneers, possibly after they became established in the disturbed vents. These results indicate that the post-eruption arrival of species from remote locales had a strong and persistent effect on communities at both disturbed and undisturbed vents.

Exploring the Ecology of Deep-Sea Hydrothermal Vents in a Metacommunity Framework

“…Larval supply of some species appears to be relatively continuous, but others arrive only episodically, hence we are unable to predict timing of recovery after a disturbance (Adams and Mullineaux, 2008;Mills et al, 2013). For instance, the arrival of a pioneer limpet Ctenopelta porifera after the 2006 EPR eruption was completely unexpected, yet had a strong and persistent effect on communities at both disturbed and near-by undisturbed vents in the region (Mullineaux et al, 2012). Limited larval supply may delay recovery even after benthic habitats have transitioned to conditions that favor later-successional species Mills et al, 2013).…”

“…Inhibition by grazing or predation was more prominent in areas of high fluid flux, productivity, and faunal densities, whilst facilitation was stronger in areas of low temperatures, productivity, and densities (Micheli et al, 2002;Mullineaux et al, 2003). Competitive exclusion or changes in larval supply may have led, for example, to replacement of the pioneer limpet Lepetodrilus tevnianus by its congener L. elevatus unrelated to changes in fluid flow (Mullineaux et al, 2012;Gollner et al, 2015).…”

“…Also within 5 years, the macrofauna and meiofauna had reached 40-70% of their pre-eruption species richness (Shank et al, 1998;Gollner et al, 2015). Following the 2006 eruption, both the macrofaunal and meiofaunal communities showed a shift in species composition over time (Mullineaux et al, , 2012Gollner et al, 2015).…”

“…At fast-spreading centers, hydrothermal fluid flux typically wanes within a few years after an eruption (Shank et al, 1998;Le Bris et al, 2006) and species diversity tends to increase (Mullineaux et al, 2012;Gollner et al, 2015). Under these conditions, it can be difficult to distinguish between effects of changing environmental conditions and biological succession.…”

Characteristics of meiofauna in extreme marine ecosystems: a review

“…In the deep sea of the North Fiji Basin in the Pacific Ocean, kinorhynchs were present both in the active hydrothermal sediments and at the control station far away from vent activities (Vanreusel et al 1997). Kinorhynchs can colonise vent sediments after a catastrophic seafloor eruption (Mullineaux et al 2012).…”