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Biol. Bull. 207: 177-182. (December 2004)
© 2004 Marine Biological Laboratory

Composition of a One-Year-Old Riftia pachyptila Community Following a Clearance Experiment: Insight to Succession Patterns at Deep-Sea Hydrothermal Vents

B. Govenar1,*, M. Freeman1, D. C. Bergquist1,{dagger}, G. A. Johnson2 and C. R. Fisher1

1 Department of Biology, 208 Mueller Laboratory, Pennsylvania State University, University Park, Pennsylvania 16802
2 University of North Carolina at Chapel Hill, Institute of Marine Sciences, Morehead City, North Carolina 28557

* To whom correspondence should be addressed. E-mail: breea{at}psu.edu

In the basalt-hosted hydrothermal vent habitat around 9°50'N on the East Pacific Rise, the vestimentiferan tubeworms Tevnia jerichonana and Riftia pachyptila (Polychaeta: Siboglinidae) commonly settle before the mussel Bathymodiolus thermophilus (Bivalvia: Mytilidae). We removed six aggregations of R. pachyptila and deployed mussels on the cleared sources of diffuse flow to test the effect of the B. thermophilus on the subsequent colonization by the tubeworms. None of the transplanted mussels persisted on the cleared sources of diffuse flow; however, aggregations of R. pachyptila grew in half of the clearances. We collected one of the aggregations of R. pachyptila along with the associated fauna for determination of relative abundance and biomass in this one-year-old community. This aggregation consisted of 647 specimens of R. pachyptila that hosted individuals of 24 species, including small individuals of T. jerichonana and B. thermophilus. The abundance of the associated fauna was numerically dominated by gastropods, and the biomass was dominated by the Alvinellid polychaete Paralvinella grasslei.

Following an eruption, the vestimentiferan tubeworms Tevnia jerichonana and Riftia pachyptila (Polychaeta: Siboglinidae) quickly colonize the basalt-hosted hydrothermal vents around 9°50'N (East Pacific Rise) and soon grow to visually dominate these habitats (1,2,3). Colonization by the vent mussel Bathymodiolus thermophilus often follows shortly, and the mussels eventually overgrow the tubeworms at most sites (2,4,5). Both tubeworms and mussels harbor sulfur-oxidizing chemoautotrophic endosymbionts, which provide the bulk of their nutrition (6,7). However, mussels have also maintained the ability to filter-feed (8), which apparently allows them to occupy a wider range of environmental conditions and better tolerate declining hydrothermal vent activity than the tubeworms (9). The mechanism of ecological succession in these hydrothermal vent habitats is not fully understood, but may be regulated by a combination of pre-settlement factors, such as the use of biogenic cues (3) and the response to geochemical changes (2), and post-settlement factors, such as physical overgrowth (4) and resource competition (5).

We conducted a manipulative experiment to test the hypothesis that the mussel B. thermophilus prevents further colonization of a vent by tubeworms. In May 1998, six aggregations of the giant tubeworm R. pachyptila were cleared from a site named Riftia Field (9°50.705'N 104°17.593'W). The original location and source of diffuse flow for each aggregation were marked and recorded on video. After the aggregations were cleared, the temperatures of the venting fluid were measured, using the low-temperature probe of the DSV Alvin, and ranged from 20–22 °C above ambient at the six locations. Then about 600 mussels were collected from a nearby site ("East Wall", 9°50.614'N 104° 17.509'W) and about 200 were deployed over each of three cleared sources of diffuse flow (treatments). Mussels were not deployed on the three other cleared areas (controls). One month later, a French expedition (HOPE98, L’Atalante/Nautile) to the same hydrothermal vent field reported that there were no mussels visible at Riftia Field (pers. obs., S. Hourdez, Station Biologique Roscoff). In April 1999, we confirmed that all but one of the mussels had disappeared without a trace, and found that aggregations of R. pachyptila had grown in three of the previously cleared diffuse flow sources. No disarticulated mussel shells were seen anywhere within this vent site, and it was not obvious whether the mussels had migrated or had been eaten. The single live mussel was observed attached to a syntactic foam marker, 50 cm above the ocean floor. In a mensurative experiment to examine the fate of the mussel deployment and the rate at which they left the area, another 200 mussels were deployed over one of the cleared (and still uncolonized) sources of diffuse flow and their movement was documented with a time-lapse camera. The temperature at this source (21 °C above ambient) had not changed significantly since the year before. After 17.5 h, the two-dimensional surface area covered by mussels increased by 32% as they began to move away from the deployment site. The fastest of the mussels moved at an average speed of 0.74 cm h–1 during the observation period. Why the adult mussels migrated away from the source of diffuse flow is unclear. Environmental conditions (i.e., sulfide concentrations or temperature) may have prevented the adult mussels from staying within the site of deployment, although the same species lives in apparently similar microhabitats on the Galapagos Rift (9) and in this vent field (10).

In April 1999, aggregations visually dominated by R. pachyptila had grown over three of the six cleared sources of diffuse flow (two treatment patches and one control). There was no evidence of recolonization at the other three, although diffuse flow was still present at every site. The temperatures ranged from 21–30 °C above ambient at the sources of the diffuse flow. Considering the almost complete absence of adult mussels in 1999 and their motility, the absence of a treatment effect on the recolonization of R. pachyptila was not surprising. There was no T. jerichonana visible in video records of any of the recolonized patches, which is unexpected because this species is often an early colonist to the basalt substrate in this area and has been hypothesized to facilitate R. pachyptila colonization (1,2,3,11). However, settlement of R. pachyptila has been previously documented on a variety of natural and artificial substrates without the prior establishment of T. jerichonana (2,11,12). In this experiment, the cleared patches had previously been colonized by R. pachyptila and were close to mature R. pachyptila aggregations, which may have facilitated conspecific settlement at this site. The apparent absence of mussels and T. jerichonana, along with the seemingly random settlement of R. pachyptila to some of the cleared sources of diffuse flow, provides additional evidence of the unpredictability of larval settlement around diffuse sources of hydrothermal flow.

At one of the recolonized patches, the base of the R. pachyptila tubes was tightly interconnected and centered directly above the venting source, which was confirmed during the previous year to be a single small hole (~ 3 cm in diameter). This aggregation of R. pachyptila was collected, intact, by its base, with the manipulator arm of Alvin, and placed into a sealed acrylic box for transport to the surface. Although some of the associated fauna were lost during the collection, review of the video record confirmed the pilot’s report that very few individuals fell from the R. pachyptila aggregation as it was placed into the collection box. Over 600 individuals of R. pachyptila were collected in this sample, along with 24 other species (Table 1). All macrofaunal species (> 500 µm) were identified, enumerated, and weighed for determination of relative abundance and biomass in this one-year-old R. pachyptila community (Table 1).


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  		Table 1 Composition of the macrofaunal assemblage associated with an aggregation of Riftia pachyptila

 
Growth rates of R. pachyptila have been estimated from the length of the tubes (1,2). However, individuals of this species can grow chitinous septa in the middle of their tubes, and they may inhabit only a portion of the total length of the tube (13,14). Therefore, tube growth may not reliably reflect animal growth. In this collection of R. pachyptila, there was a strong negative relationship between the total length of the tube and the percentage of the tube occupied by the worm (Fig. 1). Some of the largest worms occupied only 20% of their tubes, and tubes greater than 60 cm were never more than 60% occupied. The tube of R. pachyptila serves to protect the soft tissue of the animal and also to place the gas-exchange organ (the plume) in the mixing zone of diffuse hydrothermal effluent and the ambient deep-ocean water. Tube shape and length will thus be affected by the position of an individual within an aggregation and the characteristics of the vent fluid flow to that aggregation. Therefore, we consider it unlikely that the relation shown in Figure 1 will hold for R. pachyptila in other microhabitats, because the lack of direct correlation between tube length and animal length is characteristic of this species (pers. obs., C.R. Fisher). A size frequency histogram, constructed from the mass (wet weight) of all of the R. pachyptila individuals in this aggregation, suggests that this species either exhibits extremely (and we suggest unbelievably) variable individual growth rates, or that recruitment occurred throughout the previous year and included very recent settlement of R. pachyptila (Fig. 2). About 45% of the worms in the aggregation were sexually mature (with a sex ratio of 1 male to 1.3 females), and 16% weighed less than 1 g (Fig. 2). In 1997, R. pachyptila populations at the same site (Riftia Field) were similarly skewed to the smallest individuals, and the sex ratio was also around 1 to 1 (12). Negative species interactions may contribute to high juvenile mortality, but the use of biogenic cues by adult R. pachyptila may facilitate gregarious settlement and result in high population turnover (10,12).



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  		Figure 1. The percent of the Riftia pachyptila tube occupied by the individual worm decreases as the tube length increases. The occupied tube length was measured from the anterior opening of the tube to the first septum inside the tube.

 


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  		Figure 2. Histograms of the number of Riftia pachyptila individuals in 5-g size classes: (a) all individuals; (b) individuals weighing less than 10 g. At sea, wet weights of some individuals were estimated by volume displacement in a graduated cylinder and some individuals were frozen to be measured in the laboratory on a Mettler-Toledo (AG345) balance. The remaining individuals were preserved in 10% formalin, and the wet weights of a portion of these individuals were similarly estimated by volume displacement; the rest were measured on the balance. Wet weight was estimated by volume using linear regression (frozen: wet weight = 1.0256 (volume) + 0.1406, r2 = 0.995, P < 0.001; preserved: wet weight = 0.8783 (volume) + 2.310., r2 = 0.986, P < 0.001) (JMP, version 5.0, SAS).

 
This collection of an intact R. pachyptila aggregation along with the associated fauna provided an opportunity to gain insight into the structure of a R. pachyptila community of a known age. After one year, this aggregation included 647 individuals of R. pachyptila weighing 3.25 kg (ash-free dry weight) (Table 1) and contributing 96.7% of the total community biomass. The surface area of the R. pachyptila tubes provided 4.75 m2 of biogenic substrate available for colonization by other species. At least 24 macrofaunal species occupied the surfaces and interstitial spaces of the tubes, representing 13 families from phyla Annelida, Mollusca, and Arthropoda (Table 1). Colonization rates on the cleared sources of diffuse flow in this experiment were similar to those on basalt blocks that were embedded in vestimentiferan aggregations (10). However, the reassembly of the community was much faster after this clearance experiment than after an eruption and the creation of new hydrothermal vents. By the time R. pachyptila had formed dense aggregations (3.5 years post-eruption), the number of species observed was similar to the species richness in this one-year-old R. pachyptila aggregation (2).

The macrofaunal species of this community are primarily grazers and scavengers and do not rely on R. pachyptila as their primary source of nutrition (15,16). The gastropods were the most abundant of the associated fauna, accounting for 85.4% of the total 24,041 individuals. The most common species were the snail Cyathermia naticoides (40.6%) and the limpets Lepetodrilus elevatus (29.6%) and Rhyncopelta concentrica (9.0%) (Table 1). Gastropods also dominate the abundance of communities associated with the vestimentiferan Ridgeia piscesae in the basalt-hosted hydrothermal vents at the Juan de Fuca Ridge in the northeast Pacific Ocean (17,18), and Lepetodrilus spp. is often the dominant gastropod in a variety of vent habitats at the Juan de Fuca Ridge and the northern and southern East Pacific Rise (17,18,19,20,21,22,23). Although only accounting for 10.7% of the associated fauna abundance, the polychaete Paralvinella grasslei contributed the largest fraction (59.1%) of the associated fauna biomass (Table 1). In this R. pachyptila aggregation, the density of P. grasslei was considerably higher than on basalt blocks deployed for 13 months in a similar habitat at this vent field (10; unpubl. data, L. Mullineaux, Woods Hole Oceanographic Institution). P. grasslei lives in a thick mucous casing at the base of R. pachyptila tubes and may preferentially live in association with R. pachyptila. Among the species found attached to R. pachyptila tubes were small individuals of T. jerichonana (23 specimens, maximum tube length < 4 cm) and B. thermophilus (6 specimens, maximum shell length < 1.5 cm). The presence of the juvenile mussels is especially interesting in the context of the emigration of the adults transplanted to these sites. The adult mussels were deployed directly on the source of diffuse venting, which may have exceeded their tolerance range. The juvenile mussels may have settled in a more suitable habitat on the R. pachyptila tubes. Situated well above the venting source, the juvenile mussels would have been exposed to less concentrated hydrothermal flow, where the temperatures and the concentrations of reduced chemicals are lower and the oxygen concentration is higher than in fluids emanating from the basalt. In various marine environments, habitat created by foundation species can alter hydrodynamics, water chemistry, food availability, larval settlement, and biological interactions, in the addition to providing space for colonization and refuge from competitors and predators (24, for review). The data presented here suggest that R. pachyptila may modify the vent habitat to facilitate the colonization of other species. In this way, R. pachyptila seems to play an important role in the succession of species and the composition of the community in the diffuse-flow habitat of basalt-hosted hydrothermal vents at the East Pacific Rise.


   Acknowledgments
 
We thank the captain, pilots, and crews of the R/V Atlantis and the DSV Alvin for their expertise and assistance in shipboard and submersible operations on the 1998 (AT 3-19) and 1999 (AT 3-33) cruises. We are also grateful to L. Mullineaux for her contribution to the improvement of this manuscript, to S. Ivanenko and S. Hourdez for their assistance with species identification, to Steve Rose and Eileen McTague for their assistance in the laboratory, and to the Eberly College of Science, Pennsylvania State University, for the support of undergraduate participation in this project. This work was funded by the National Science Foundation grants OCE-9712808 (to CRF), OCE-9712233 (to L. Mullineaux), and OCE-9712809 (to C. Peterson).


   Footnotes
 
Received 28 April 2004; accepted 4 October 2004.

{dagger} Present address: Department of Fisheries and Aquatic Sciences, University of Florida, Gainesville, FL 32653. Back


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