Larvae from afar colonize deep-sea hydrothermal vents after a catastrophic eruption

Abstract

The planktonic larval stage is a critical component of life history in marine benthic species because it confers the ability to disperse, potentially connecting remote populations and leading to colonization of new sites. Larval-mediated connectivity is particularly intriguing in deep-sea hydrothermal vent communities, where the habitat is patchy, transient, and often separated by tens or hundreds of kilometers. A recent catastrophic eruption at vents near 9 degrees 50'N on the East Pacific Rise created a natural clearance experiment and provided an opportunity to study larval supply in the absence of local source populations. Previous field observations have suggested that established vent populations may retain larvae and be largely self-sustaining. If this hypothesis is correct, the removal of local populations should result in a dramatic change in the flux, and possibly species composition, of settling larvae. Fortuitously, monitoring of larval supply and colonization at the site had been established before the eruption and resumed shortly afterward. We detected a striking change in species composition of larvae and colonists after the eruption, most notably the appearance of the gastropod Ctenopelta porifera, an immigrant from possibly more than 300 km away, and the disappearance of a suite of species that formerly had been prominent. This switch demonstrates that larval supply can change markedly after removal of local source populations, enabling recolonization via immigrants from distant sites with different species composition. Population connectivity at this site appears to be temporally variable, depending not only on stochasticity in larval supply, but also on the presence of resident populations.

Fig. 1.

Locations of vents and sample sites on the East Pacific Rise in the region of the eruption. Symbols designate vent sites (yellow circles), sediment traps (inverted triangles), and colonization experiments (squares) (blue = pre-eruption, red = post-eruption). Blue line outlines the extent of lava extruded in the 2005–2006 eruption (22). Bathymetry of ridge (53) is contoured at 10-m intervals. Map courtesy of S. A. Soule.

Fig. 2.

Larval supply measured in sediment traps. Traps sampled before the eruption (November 25, 2004, to April 21, 2005, at 7-day intervals; blue bars) near East Wall vent and after (July 1 to November 4, 2006; 6-day intervals; red bars) near P-vent. Supply (daily downward flux of larvae into 0.5-m² trap opening) displayed for the six most abundant species/groups at either site that also were found as colonists: (A) Cyathermia naticoides, (B) Lepetodrilus spp; (C) Gorgoleptis spiralis, (D) Bathymargarites symplector, (E) Gorgoleptis emarginatus, (F) Ctenopelta porifera. Mean flux of each species except G. emarginatus changed significantly (P < 0.05, MANOVA and ANOVA; Table S2) after the eruption. Larval individuals of the five described lepetodrilid species in this region (Lepetodrilus elevatus, L. pustulosus, L. ovalis, L. cristatus, and L. tevnianus) were not distinguishable morphologically.

Fig. 3.

nMDS of species composition of larvae and colonists. The proximity of samples corresponds to the similarity in their species composition. Analysis conducted on Pearson correlation of fourth-root transformed abundance. (A) Larvae (excluding polychaetes) in sediment traps before (blue dots) and after (red dots) eruption; label designates site (E = East Wall, P = P-vent) and cup interval; Kruskal stress = 0.15. (B) Colonists (gastropods only) on blocks before the eruption (blue dots) and on sandwiches after (red dots); label designates site (WH = Worm Hole, TA = Tica; TY = Ty/Io, P = P-vent), environment (H = hot, W = warm), and replicate; Kruskal stress = 0.073. Mean species or species-group abundances listed in Table S3.

Fig. 4.

Species composition of vent gastropod colonists and larvae. All gastropods were identified to species except larval and small juvenile Lepetodrilus, which could only be identified to genus. Jagged line separates pre- (Left) and post-eruption (Right) samples. (A) Colonists in hot vent environment before eruption at Worm Hole and Tica vents and after eruption at P-vent. Values are average relative abundances (±SE; n = 3) of seven most common species or species groups (those >2% of all vent gastropods at any of three sites). (B) Colonists in warm vent environment before eruption at Worm Hole and after eruption near Ty/Io vent. Values are average relative abundances (±SE; n = 3) of six most abundant species/groups (those >2% of all vent gastropods at either of two sites). (C) Larval supply in sediment traps before eruption at East Wall and Choo Choo vents and after eruption at P-vent. Values are average relative abundances (±SE; n = 21) of six most common species/groups that are also found as colonists.