SEARCH

SEARCH BY CITATION

Keywords:

  • Bathynerita naticoidea;
  • behavior;
  • brine pool;
  • cold seep;
  • Methanoaricia dendrobranchiata;
  • osmoregulation;
  • salinity tolerance

Abstract

  1. Top of page
  2. Abstract
  3. Problem
  4. Material and Methods
  5. Results
  6. Discussion
  7. Summary
  8. Acknowledgements
  9. References

Bathynerita naticoidea (Gastropoda: Neritidae) and Methanoaricia dendrobranchiata (Polychaeta: Orbiniidae) are two of the most abundant invertebrates associated with cold-seep mussel beds in the Gulf of Mexico. At the methane seep known as Brine Pool NR-1 (27 °43.415 N, 91 °16.756 W; 650 m depth), which is surrounded by a broad band of mussels (Bathymodiolus childressi), these species have distinctly different patterns of abundance, with the gastropod being found mostly at the outer edge of the mussel bed (average density in November 2003: 817 individuals·m−2 in outer zone, 20·m−2 in inner zone) and the polychaete being found almost exclusively near the inner edge (average density in November 2003: 3155 individuals·m−2 in inner zone, 0·m−2 in outer zone), adjacent to the brine pool itself. The salinity of the brine pool exceeds 120, so we hypothesized that M. dendrobranchiata should be more tolerant of high salinities than B. naticoidea. The opposite proved to be true. The gastropods were capable of withstanding salinities at least as high as 85, whereas the polychaetes died at salinities higher than 75. Both species were osmoconformers over the range of salinities (35–75) tested. Behavioral responses of B. naticoidea to salinities of 50, 60, and 70 were investigated in inverted vertical haloclines. Gastropods generally did not enter water of salinity greater than 60, but tolerated short periods at 60. Behavioral avoidance of brine should limit the vertical distribution of B. naticoidea in the inner zone to the top 2.5–5 cm of the mussel bed. Behavior is also a likely (though unproven) mechanism for controlling horizontal distribution of this species across the mussel bed. Methanoaricia dendrobranchiata can tolerate short excursions into the brine, but probably avoids hypersaline conditions by aggregating on the tops of the mussels.


Problem

  1. Top of page
  2. Abstract
  3. Problem
  4. Material and Methods
  5. Results
  6. Discussion
  7. Summary
  8. Acknowledgements
  9. References

Dense assemblages of chemosynthetic organisms were first reported along the Louisiana continental slope in the mid-1980s (Kennicutt et al. 1985). Mussel beds and tubeworm bushes in this region provide food and habitat for a diverse community of endemic and vagrant consumers including gastropods, alvinocarid shrimp, galatheid crabs, and orbiniid polychaetes (MacAvoy et al. 2002; Bergquist et al. 2005). Among the best-studied seeps in this region is Brine Pool NR-1 (27 °43.4157 N, 91 °16.756 W, ∼650 m depth), a methane-enriched lake of brine (salinity 121.35) surrounded by a dense bed of the mussel Bathymodiolus childressi (Childress et al. 1986; MacDonald et al. 1990). The mussel community is from 3 to 7 m in width, covering an area of ∼540 m2 and can be divided into two distinct zones, the inner and outer zones, that differ both chemically and faunistically and are separated by a transitional middle ‘zone’ (MacDonald et al. 1990; Smith et al. 2000; Bergquist et al. 2005). In the inner zone, mussels overhang the edge of the pool and are bathed in brine (Fig. 1) whereas mussels in the outer zone rest on soft sediment (Smith et al. 2000; Arellano, unpublished data).

image

Figure 1.  Photograph of the inner edge of the mussel bed at Brine Pool NR-1. The black regions of the photograph are brine at a salinity of approximately 120. Note that the proximal ends of many mussels are submerged in brine. A dense aggregation of the orbiniid polychaete Methanoaricia dendrobranchiata is visible in the middle of the photograph. Scale bar: approximately 5 cm.

Download figure to PowerPoint

Two of the most common invertebrates associated with brine-seep mussels are the neritid gastropod Bathynerita naticoideaClarke 1989 and the orbiniid polychaete Methanoaricia dendrobranchiataBlake 2000. Methanoaricia dendrobranchiata is much more abundant in the inner zone than in the outer zone (Bergquist et al. 2005). Bathynerita naticoidea, though found in all zones, is more abundant near the outside edge of the mussel bed (Bergquist et al. 2005). These differences in distribution correlate with a number of physical and chemical gradients (Smith et al. 2000; Bergquist et al. 2005). The inner zone is characterized by high methane and oxygen concentrations (>200 and ≤160 μm, respectively) and hydrogen sulfide too low to detect (Smith et al. 2000). The outer zone of the mussel bed has similar methane concentrations, lower average oxygen levels (sometimes <50 μm), and very high hydrogen sulfide (>1000 μm) (Smith et al. 2000). The vertical salinity gradient at the brine pool interface is very abrupt, with a salinity of about 120 in the pool itself and about 35 just above the pool surface. As uncontaminated water samples are difficult to collect from the interstices of the mussel bed, we do not have a clear picture of the salinity gradient across the bed. Smith et al. (2000) attempted to measure salinity at three depths within the mussel bed and in all three zones, but they do not report complete data because of artifacts associated with the sampling method. Nevertheless, they do note that the proportion of samples having elevated salinities (above 39) at a depth of 10 cm from the tops of the mussels decreased from the inner to the outer zone and also noted that the salinity 2.5 cm below the tops of the mussels was never elevated in the outer two zones (Smith et al. 2000).

Bathynerita naticoidea is the most abundant gastropod at hydrocarbon seeps in the Gulf of Mexico and on the Barbados accretionary prism at depths ranging from 400 to 2100 m (Carney 1994; Olu et al. 1996; Zande & Carney 2001; Bergquist et al. 2005). A neritid similar to B. naticoidea has been found in Miocene deposits in Italy and also at middle Eocene fossil seeps in western Washington, USA, suggesting a long history of association with cold seeps (Taviani 1994; Squires & Goedert 1996). Bathynerita naticoidea grazes on methanotrophic bacteria and detritus from hard substrata, primarily the shells of Bathymodiolus childressi (Zande & Carney 2001). Methanoaricia dendrobranchiata is a monogeneric species known only from seeps in the Gulf of Mexico (Blake 2000). Its respiratory adaptations (Hourdez et al. 2001, 2002) and spermiogenesis have been described (Eckelbarger & Young 2002) but other aspects of its biology remain poorly known. This species often forms dense aggregations that drape over the tops of mussels (Fig. 1).

We undertook a comparative study to determine if the distinctly different distributions of B. naticoidea and M. dendrobranchiata reflect physiological or behavioral attributes of the two species. As M. dendrobranchiata is found in closer proximity to the brine, we hypothesized that this species might be more tolerant of high salinities and that it might have better osmoregulatory abilities than B. naticoidea. We also hypothesized that the aggregating behavior of M. dendrobranchiata might reduce adverse effects of high salinity, either by reducing exposure of permeable surfaces to the brine or by making it easier for individuals to remain above the brine, at the surface of the mussel bed. Finally, we tested the ability of B. naticoidea to avoid high-salinity water behaviorally.

Material and Methods

  1. Top of page
  2. Abstract
  3. Problem
  4. Material and Methods
  5. Results
  6. Discussion
  7. Summary
  8. Acknowledgements
  9. References

Field distribution

To determine the abundances of B. naticoidea and M. dendrobranchiata, we used a Johnson-Sea-Link submersible to collect discrete quantitative samples of mussels and associated fauna from the three zones of the brine pool mussel bed during cruises in November 2003 and August 2006. On the 2003 cruise, a 50 × 50 cm PVC quadrat was placed on the mussel bed and all organisms found within that quadrat were removed with a mechanical clam-bucket scoop and a suction hose. Only one such quadrat sample was taken from each zone because of dive-time constraints. However, we also collected two additional sets of samples during the same cruise and 3 sets (n=3/zone) in 2006 using the clam-bucket scoop as a quantitative sampling device. This scoop is similar in operation to a benthic grab and samples 345 cm2. Before taking each sample, we removed mobile fauna from within the sample area using a suction hose on the submersible's manipulator arm. We then took two adjacent grabs (total area of 690 cm2 and removed any organisms in the resulting hole with the suction hose. Our data on distribution were compared with those of Bergquist et al. (2005), who used similar quantitative collection techniques at the same site nearly one decade earlier.

Salinity tolerances

Salinities were measured using a hand-held refractometer and are expressed without dimensions or units, as recommended by UNESCO (1985). We mixed seawater brine with seawater to obtain the desired salinities for experiments. The brine was obtained by freezing seawater, then siphoning off the high-density melt water as the ice thawed. Using this method, we were able to obtain salinities as high as 85.

We tested the salinity tolerance of B. naticoidea in two different ways. In the first series of experiments, we held gastropods in 160-ml culture dishes completely filled with seawater of various salinities (55, 65, 75, 85) and covered with glass Petri dishes to prevent escape. Each dish contained five individuals and each salinity treatment was replicated three times. We tested gastropods at two lower salinities (35, 45) on a different day with 10 individuals per dish. Gastropods were held in all treatments for 15 h then allowed to recover in water of salinity 35 for 18 h. In the second experiment, gastropods (15 per salinity) were incubated in individual Falcon tubes, each containing 50 ml of seawater (salinities: 35, 55, 65, 75, 85), for 15 h. In this experiment, animals were scored immediately for survival, then some were used for osmolality measurements as described below. In all experiments, we tested for survival by prodding the foot or operculum with a blunt probe and noting any responses. If B. naticoidea did not respond by moving its foot or pulling down its operculum, then it was counted as dead.

We tested the salinity tolerance of M. dendrobranchiata by holding individual polychaetes in separate Styrofoam cups, each containing 60 ml of seawater at the following salinities: 35, 45, 55, 65, 75, 85. Each salinity treatment was replicated four times and run for 15 h. We tested the potential effect of aggregation on salinity tolerance by holding groups of five polychaetes in cups (four replicate cups per treatment) at salinities of 35, 75 and 85. In all experiments, polychaetes were transferred back into seawater at a salinity of 35 and observed over the next 18 h for signs of activity. Polychaetes that appeared inactive were prodded with forceps. If repeated prodding did not stimulate any movement, then the polychaetes were scored as dead.

Osmoregulatory ability

We tested osmoregulatory ability of B. naticoidea by comparing the osmolality of hemolymph from gastropods incubated for 15 h at various salinities to the osmolality of the seawater in which they were incubated. Ten gastropods were sampled at each of two salinities, 35 and 75, and three gastropods were sampled at 55. Following exposure to their respective salinity treatments, gastropods were removed from their shells and blotted dry on a paper towel, then punctured in the foot region to obtain hemolymph. The hemolymph from each gastropod was absorbed on a standardized disc of Whatman No. 1 filter paper. Filter disks were placed immediately into a Vapro 5520 vapor-pressure osmometer for analysis. Mean osmolalities were compared among treatments using one-way ANOVA.

Experiments on osmoregulation in M. dendrobranchiata were performed when no osmometer was available. As an alternative to direct measures of coelomic osmotic pressure, we measured changes in body mass of polychaetes that were incubated in seawater brine for 1–6 h (Oglesby 1978). Six individual polychaetes were blotted briefly on a paper towel then weighed on a top-loading balance sensitive to 0.01 g. Each polychaete was then assigned randomly to one of six styrofoam cups containing brine at a salinity of 75. One randomly selected polychaete was removed each hour, blotted, then weighed again. We tested the relationship between weight loss and exposure time for linearity with regression analysis.

Behavioral responses of B. naticoidea to high salinities

Bathynerita naticoidea generally move upward in laboratory tanks, spending most of their time at the air/water interface. We exploited this behavior to investigate the responses of individual gastropods to high salinities. Gastropods were placed below inverted haloclines and allowed to crawl upward to determine if they would enter waters of three different high salinities.

Experimental inverted haloclines were constructed in large glass test tubes (25 × 200 mm) in a 7 °C cold room. Blue food coloring (FD&C Blue #1 dye) was used to mark the depths of all haloclines. In each case, the higher salinity was at the top and the lower ambient salinity (always 35) was at the bottom. To make stable inverted haloclines, the density of the ambient salinity (bottom layer) water was increased by 0.05 kg·m−3 above that of the high salinity water by adding PercollTM (Amersham Pharmacia Biotech), a sterile solution composed of silica beads (15–30 nm) coated with polyvinylpyrrolidone, a non-toxic material with an osmolality of <25 mOs·kg−1 H2O. The osmolality of each PercollTM solution was checked with a Vapro 5520 vapor pressure osmometer and osmolality was corrected where necessary by the addition of seawater or brine. The three halocline treatments had top-layer salinities of 50, 60 and 70 and are referred to hereafter as the 50-halocline, 60-halocline, and 70-halocline treatments.

Three isocline (control) treatments were also constructed, with dense seawater as the bottom layer and ambient seawater (salinity: 35) as the top layer, to act as controls for the addition of PercollTM. In these isoclines, the densities of the bottom layers were adjusted with Percoll to match the densities of the bottom layers in the corresponding halocline treatments (Table 1).

Table 1.   Salinity and density (units of kg·m−3) conditions in the isocline and halocline experiments.
treatment nametop layerbottom layer
salinitydensitysalinitydensity
  1. *Percoll was added to achieve the desired density.

50-halocline501.040351.045*
50-isocline351.025351.045*
60-halocline601.045351.050*
60-isocline351.025351.050*
70-halocline701.050351.055*
70-isocline351.025351.055*

Each halocline treatment was run concurrently with its corresponding isocline treatment, using 20 individual gastropods in separate test tubes for each treatment. There were three different pairs of treatment (top salinities of 50, 60, 70) and each was repeated twice for a total of six trials (where trial is defined as a set of experiments run on one occasion). During a trial, one randomly selected gastropod was gently dropped into each tube, taking care not to disrupt the haloclines. After 1 h, the position of each gastropod was recorded, then categorized as top, middle, or bottom. Each test tube was divided into 40 units. The top bin included the top 15 units, the middle bin included 5 units immediately above and below the halocline (10 units total), and the bottom bin consisted of the bottom 15 units.

The responses of B. naticoidea to haloclines were initially analyzed as a three-way mixed model ANOVA with treatment and salinity as fixed factors and trial as a random factor. In this analysis, the ‘trial’ factor was not significant, so data were pooled across trials and reanalyzed by two-way ANOVA, with treatment and salinity as fixed factors.

Results

  1. Top of page
  2. Abstract
  3. Problem
  4. Material and Methods
  5. Results
  6. Discussion
  7. Summary
  8. Acknowledgements
  9. References

Field Distribution

The neritid gastropod B. naticoidea and the orbiniid polychaete M. dendrobranchiata showed consistently different patterns of distribution across the brine pool mussel bed (Fig. 2), with B. naticoidea occurring much more abundantly in the middle and outer zones and M. dendrobranchiata being one to two orders of magnitude more abundant at the pool edge than in the middle or outer zones.

image

Figure 2.  Densities of Bathynerita naticoidea and Methanoaricia dendrobranchiata in the inner, middle and outer zones of the Brine Pool. Original data are from two cruises in November 2003 and August 2006. Data from Bergquist et al. (2005) are plotted for comparative purposes. Error bars are 95% confidence intervals.

Download figure to PowerPoint

Bergquist et al. (2005) also collected quantitative samples of these two species in the same zones at Brine Pool NR-1. Their data (Fig. 2), collected nearly a decade earlier than our collections, show patterns of distribution similar to the ones we found, suggesting that these patterns are consistent over time.

Salinity Tolerance

All B. naticoidea incubated in salinity treatments of 35, 45 and 55 survived the experimental exposures (Fig. 3) and crawled actively around the bowls. Gastropods exposed to a salinity of 65 appeared stressed, often lying upside down with the operculum open. At salinities of 75 and 85, all large animals spent the entire incubation period with their opercula closed, though a few of the smallest individuals remained open and crawled about in the dishes. Gastropods from all salinity treatments that were transferred into ambient (salinity 35) seawater recovered and resumed locomotion within several hours. In the experiment where individuals were used for osmolality measurements immediately after their incubation period, 25% of the gastropods at salinity 75 were scored as dead (Fig. 3). However, it is not known if these individuals would have recovered had they been moved back into ambient seawater.

image

Figure 3.  Survival of Bathynerita naticoidea and Methanoaricia dendrobranchiata incubated as individuals and in groups for 15 h in various salinities. Error bars are 95% confidence intervals. Asterisks indicate absence of treatments.

Download figure to PowerPoint

All M. dendrobranchiata survived at salinities up to 65 (Fig. 3). One polychaete died in each density treatment (clumped and individual) at a salinity of 75 and no polychaetes survived exposure to water of salinity 85 (Fig. 3). Time of death for polychaetes exposed to the highest salinity varied between 4 and 15 h. Polychaetes incubated in groups demonstrated their normal clumping behavior at a salinity of 35 but those held at a salinity of 75 became lethargic and did not aggregate.

Osmoregulatory ability

The hemolymph osmolalities of B. naticoidea incubated for 15 h at salinities of 35, 55 and 75 were all virtually identical to the osmolalities of the respective seawater solutions in which they were incubated (Fig. 4) and were all significantly different from each other (one-way ANOVA, F2,42 = 170.89, P < 0.001), indicating a lack of osmoregulatory ability. Methanoaricia dendrobranchiata held at salinity 75 lost over 30% of their body mass during the first hour and more than 45% of their body mass by the end of the 6-h experiment (Fig. 4). The relationship between mass loss and exposure time was significantly linear (r2 = 0.89, P = 0.004), suggesting that these polychaetes are osmoconformers.

image

Figure 4.  Top panel: Hemolymph osmolality of Bathynerita naticoidea incubated at three salinities for 15 h. The points and line indicate empirically measured osmolalities of seawater at salinity increments of 5. Error bars are standard deviations. Bottom panel: Loss of body mass in Methanoaricia dendrobranchiata incubated for 1–6 h in brine of salinity 75.

Download figure to PowerPoint

Responses of B. naticoidea to haloclines

The behavior of B. naticoidea differed between the isocline and halocline treatments as indicated by a significant interaction in the two-way ANOVA (F2,233 = 3.42, P =0.034) at haloclines above 50. The 60- and 70-halocline treatments were both significantly different from the 50-halocline treatment (P = 0.001, 0.013, respectively, by Bonferroni post-hoc test).

Between 70% and 87.5% of the gastropods in the isocline treatments crawled to the surface (Fig. 5) and most came to rest with 2–5 mm of their body protruding from the water. In the 50-halocline treatment, 65% of the gastropods crawled to the top of the tube, stopping at the air–water interface. In the 60-halocline treatment, only 12.5% of the gastropods crawled through the high-saline water to the surface. No gastropods were found in the top layer of the 70-halocline treatment.

image

Figure 5.  Final positions of Bathynerita naticoidea along vertical test tubes containing inverted haloclines and their corresponding isocline controls. Salinities in the upper layers of the three haloclines (‘top salinities’) were 50, 60 and 70. Underlying layers of salinity 35 were increased in density using Percoll to maintain stability of the haloclines. The actual densities and salinities of all layers are given in Table 1. Error bars are standard deviations.

Download figure to PowerPoint

In the 60- and 70-halocline treatments, gastropods were usually found just below the halocline, with a few millimeters of foot or tentacle extending into the high salinity water. Interestingly, 22.5% of the gastropods in the 60-halocline treatment were found within 10 mm below the halocline and another 25% were at the halocline with part of their body or shell in each layer. In the 70-halocline treatment, 35% of the gastropods were within 10 mm below the halocline and 35% were at the halocline.

Discussion

  1. Top of page
  2. Abstract
  3. Problem
  4. Material and Methods
  5. Results
  6. Discussion
  7. Summary
  8. Acknowledgements
  9. References

Most species living at Brine Pool NR-1 are more abundant in the inner zone than in the outer zone (Bergquist et al. 2005; Arellano & Young, unpublished data). The orbiniid polychaete M. dendrobranchiata is perhaps the most dramatic example of this pattern. Although this species is sometimes found in the middle and outer zones, its density is typically one to two orders of magnitude higher in the inner zone. This abundance pattern is very different from that of B. naticoidea, which is typically more abundant, sometimes by an order of magnitude or more, in the outer zone (Fig. 2). Abundance of this species in the middle zone was highly variable among collection dates and even among samples within collection dates (Fig. 2), a fact that reflects the patchy distribution of B. naticoidea and supports the conclusion made by Smith et al. (2000) that the middle zone is not a distinct zone, but a transitional area between the inner and outer zones.

Based on the dramatic distributional differences between the two species, we first hypothesized that the polychaete should be more tolerant of high salinities and better able to osmoregulate than the gastropod. With the evidence now at hand, we reject both hypotheses. Bathynerita naticoidea tolerated higher salinities than M. dendrobranchiata over the 15-h tested, and neither animal was able to regulate its internal osmolality.

Bathynerita naticoidea are euryhaline and can tolerate salinities at least as high as 85 for a period of time (Fig. 3), but animals are stressed at salinities above 65 and probably survive higher salinities only by pulling the operculum tightly shut. Our evidence shows that this species has no osmoregulatory ability at high salinities (Fig. 4). Most neritid gastropods live in warm, tropical, shallow-water habitats and many have life cycles that include both freshwater and saltwater stages (Fretter & Graham 1962; Clarke 1989). At low salinities, some neritids have some osmoregulatory ability, with osmoregulation in freshwater neritids occurring in the proximal excretory limb of the left kidney and, to a lesser degree, in the smooth-walled distal limb (Andrews 1988). Marine neritid species such as Nerita fulgurans, however, often have blood that is isosmotic with urine, suggesting that they osmoconform (Fretter & Graham 1962; Andrews 1988). Osmoconformity is, in fact, the rule among marine prosobranchs (reviewed by Little 1981; Burton 1983). Littorinid and acmaeid gastropods living in the intertidal zone have been shown to withstand desiccation for up to several months, during which time their hemolymph may attain solute concentrations equivalent to 300% seawater (Wolcott 1973; Emson et al. 2002). This incredible ability to tolerate very high internal solute concentrations is also apparent in B. naticoidea, a gastropod occupying a very different kind of extreme condition.

We noted at least three behaviors that protect B. naticoidea from high salinity. First, the gastropods can survive exposure to brine for many hours by tightly closing the operculum. Second, they typically move upward, a behavior that should keep them on the top of the mussels where salinity is the lowest. Third, they avoid entering water of salinity higher than 60. In the inner zone, brine is found within 2.5 cm of the top of the mussels (Smith et al. 2000); elsewhere in the mussel bed, elevated salinities have been measured at depths of 5 and 10 cm. The behavioral responses of B. naticoidea would effectively limit the vertical distribution of B. naticoidea to the very tops of mussels in the inner zone, but they would have more habitat available to them in the outer zone where brine is either deeper or non-existent.

The orbiniid polychaete M. dendrobranchiata tolerated salinities only up to 75 over a 15-h trial. Nevertheless, they were able to tolerate several hours of exposure to a salinity of 85, suggesting that they can endure brief excursions into the brine that lies just below their habitat.

Polychaetes are typically marine, but representatives are found in fresh and brackish waters (e.g., Oglesby 1978; Tait et al. 1981; Qiu & Qian 1998; Pechenik et al. 2000) and a few are known to inhabit hypersaline lakes. Cirriformia spirabrancha from California and Polydora ligni from the Laguna Madre of Texas have been found in water of salinity 75 and Nephtys hombergi occurs at salinities as high as 50 in the Black Sea (Dice 1969; Bayly 1972). Salt and ion balance in polychaetes has been reviewed by Dales (1967), Bayly (1972) and Oglesby (1978). The last author provides extensive tables of species that have been exposed experimentally to various salinities. Virtually all polychaetes tested at higher than their normal salinities are osmoconformers (e.g., Skaer 1964; Bayly 1972; Oglesby 1978; Ferraris et al. 1994), so the rapid loss of mass we observed in M. dendrobranchiata incubated at a salinity of 75 is not unexpected. A few species of polychaetes living at low salinity or in fresh water have some ability to hyperosmoregulate (e.g., Tait et al. 1981; Oglesby et al. 1982). Not having the physiological ability to survive long periods in brine, we suspect that M. dendrobranchiata, like B. naticoidea, must use behavioral mechanisms to avoid prolonged exposure to the hypersaline conditions that exist within millimeters of its normal habitat. Although aggregation behavior does not protect polychaetes that are immersed in high salinity water (they ceased aggregating when immersed in brine), it is possible that polychaetes in large clumps spread their collective surface area across the tops of the mussels in such a way as to remain out of the brine (Fig. 1).

Although both species have behaviors that may be used for avoidance of hypersaline conditions, our evidence is insufficient to infer the mechanisms by which horizontal patterns of distribution are maintained. At the Brine Pool, chemical gradients in salinity, oxygen, methane, and hydrogen sulfide could influence animal distributions either individually or interactively. The area immediately adjacent to the brine pool has more oxygen and less hydrogen sulfide than the outer zone, an observation that has been invoked as a possible explanation for higher abundances of many species in the inner zone (Smith et al. 2000; Bergquist et al. 2005). Predation or competition at the inner edge of the pool could also play roles in setting and maintaining spatial patterns.

There is a very distinct halocline at the edge of the pool. Mussels residing near the edge of the pool, including abundant small individuals, appear to be in contact with brine having a salinity in excess of 120 (Fig. 1), while their siphons are exposed to normal seawater of salinity 35–37 (Smith et al. 2000). Vagrant animals crawling on and between the mussels must therefore have frequent contact with high-salinity water. Interstitial salinity across the mussel bed has not been measured successfully (Smith et al. 2000), so we do not know if a salinity gradient extends across the entire bed. Even without a gradient, however, behavioral avoidance of brine could explain the low densities of B. naticoidea in the inner zone. Our data on salinity tolerances provide no satisfactory explanation for the higher density of M. dendrobranchiata near the edge of the brine pool than in the outer zone.

Summary

  1. Top of page
  2. Abstract
  3. Problem
  4. Material and Methods
  5. Results
  6. Discussion
  7. Summary
  8. Acknowledgements
  9. References

In the mussel bed that rings Brine Pool NR-1 cold seep in the Gulf of Mexico, the neritid gastropod B. naticoidea is the most abundant species in the outer and middle zones of the bed, whereas the orbiniid polychaete M. dendrobranchiata is the most abundant in the inner zone, where it resides very near brine with a salinity exceeding 120. Paradoxically, B. naticoidea had a higher salinity tolerance than M. dendrobranchiata. The gastropod survived salinities of 85 by closing its operculum. This species also avoided passing through haloclines into salinity higher than 60. Salinity tolerances do not explain the differences in distribution, but behavior seems to play a role in salinity avoidance for both species.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Problem
  4. Material and Methods
  5. Results
  6. Discussion
  7. Summary
  8. Acknowledgements
  9. References

We thank the crews of the R/V Seward Johnson I & II and the Johnson Sea Link submersibles for their expertise in collecting samples. Maya Wolf and Tracey Smart assisted with laboratory experiments and Sandra Brooke provided advice and assistance in the field and laboratory. We thank Bob Carney for providing bunks and dive time on one of his research cruises and for sharing his understanding of cold-seep organisms. This research was funded by NSF grant OCE-0243688 to the University of Oregon. Most of the data on B. naticoidea were part of a M.S. thesis by A. Van Gaest. Data on M. dendrobranchiata came from a student project by J. Young and A. Helms, who participated in the Univ. of Oregon Deep-sea Biology Course with assistance from Oregon Seagrant. Data on distribution of the two species are parts of a dissertation by S. Arellano. We thank Nora Terwiliger for the use of a vapor-pressure osmometer.

References

  1. Top of page
  2. Abstract
  3. Problem
  4. Material and Methods
  5. Results
  6. Discussion
  7. Summary
  8. Acknowledgements
  9. References
  • Andrews E.B. (1988) Excretion systems of mollusks. In: TruemanE.R., ClarkeM.R. (Eds), The Mollusca, Vol. 11. Form and Function. Academic Press, Orlando: 381448.
  • Bayly I.A.E. (1972) Salinity tolerance and osmotic behavior of animals in athalassic saline and marine hypersaline waters. Annual Review of Ecology and Systematics, 3, 232268.
  • Bergquist D.C., Fleckenstein C., Knisel J., Begley B., MacDonald I.R., Fisher C.R. (2005) Variations in seep mussel bed communities along physical and chemical environmental gradients. Marine Ecology Progress Series, 293, 99108.
  • Blake J.A. (2000) A new genus and species of polychaete worm (Family Orbiniidae) from methane seeps in the Gulf of Mexico, with a review of the systematics and phylogenetic interrelationships of the genera of Orbiniidae. Cahiers de Biologie Marine, 41, 435449.
  • Burton R.G. (1983) Ionic regulation and water balance. In: SaleuddinA.S.M., WilberK.M. (Eds), The Mollusca. Vol. 5, Physiology, Part 2. Academic Press, New York: 291352.
  • Carney R.S. (1994) Consideration of the oasis analogy for chemosynthetic communities at Gulf of Mexico hydrocarbon vents. Geo-Marine Letters, 14, 149159.
  • Childress J.J., Fisher C.R., Brooks J.M., Kennicutt M.C. II, Bidigare R., Anderson A. (1986) A methanotrophic marine molluscan symbiosis: mussels fueled by gas. Science, 233, 13061308.
  • Clarke A.H. (1989) New mollusks from undersea oil seep sites off Louisiana. Malacology Data Net, 2, 122134.
  • Dales H.P. (1967) Annelids. Hutchinson, London: 200 pp.
  • Dice J.F. Jr (1969) Osmoregulation and salinity tolerance in the polychaete annelid Cirriformia spirabrancha (Moore, 1904). Comparative Biochemistry and Physiology, 28, 13311343.
  • Eckelbarger K.J., Young C.M. (2002) Spermiogenesis and modified sperm morphology in the ‘‘seep worm’’Methanoaricia dendrobranchiata (Polychaeta: Orbiniidae) from a methane seep environment in the Gulf of Mexico: Implications for fertilization biology. Biological Bulletin, 203, 134143.
  • Emson R.H., Morritt D., Andrews E.B., Young C.M. (2002) Life on a hot dry beach: behavioural, physiological and ultrastructural adaptations of the littorinid gastropod Cenchritis (Tectarius) muricatus. Marine Biology, 140, 723732.
  • Ferraris J.D., Fauchald K., Kensley B. (1994) Physiological responses to fluctuation in temperature or salinity in invertebrates. Adaptations of Alpheus viridari (Decapoda, Crustacea), Terebellides parva (Polychaeta) and Golfingia cylindrata (Sipunculida) to the mangrove habitat. Marine Biology, 120, 397406.
  • Fretter V., Graham A. (1962) British Prosobranch Molluscs, Their Functional Anatomy and Ecology. The Ray Society, London.
  • Hourdez S., Frederick L., Schernecke A., Fisher C.R. (2001) Functional respiratory anatomy of a deep-sea orbiniid polychaete from the Brine Pool NR-1 in the Gulf of Mexico. Invertebrate Biology, 120, 2940.
  • Hourdez S., Weber R.E., Green B.N., Kenney J.M., Fisher C.R. (2002) Respiratory adaptations in a deep-sea orbiniid polychaete from Gulf of Mexico Brine Pool NR-1: metabolic rates and hemoglobin structure/function relationships. Journal of Experimental Biology, 205, 16691681.
  • Kennicutt M.C., Brooks J.M., Bidigare R.R., Fay R.R., Wade T.L., McDonald T.J. (1985) Vent-type taxa in a hydrocarbon seep region on the Louisiana slope. Nature, 317, 351353.
  • Little C. (1981) Osmoregulation and excretion in prosobranchs, part 1. Physiology. Journal of Molluscan Studies, 47, 221247.
  • MacAvoy S.E., Carney R.S., Fisher C.R., Macko S.A. (2002) Use of chemosynthetic biomass by large, mobile, benthic predators in the Gulf of Mexico. Marine Ecology Progress Series, 225, 6578.
  • MacDonald I.R., Reilly J.F. II, Guinasso N.L. Jr, Brooks J.M., Carney R.S., Bryant W.A., Bright T.J. (1990) Chemosynthetic mussels at a brine-filled pockmark in the northern Gulf of Mexico. Science, 248, 10961099.
  • Oglesby L.C. (1978) Salt and water balance. In: MillP.J. (Ed.), Physiology of Annelids. Academic Press, London: 555658.
  • Oglesby L.C., Mangum C.P., Heacox A.E., Ready N.E. (1982) Salt and water balance in the polychaete Nereis virens. Comparative Biochemistry and Physiology, 73A, 1519.
  • Olu K., Sibuet M., Harmegnies F., Foucher J.P., Fiala Médioni A. (1996) Spatial distribution of diverse cold seep communities living on various diapiric structures of the southern Barbados prism. Progress in Oceanography, 38, 347376.
  • Pechenik J.A., Berard R., Kerr L. (2000) Effects of reduced salinity on survival, growth, reproductive success, and energetics of the euryhaline polychaete Capitella sp. I. Journal of Experimental Marine Biology and Ecology, 254, 1935.
  • Qiu J.-W, Qian P.-Y. (1998) Combined effects of salinity and temperature on juvenile survival, growth and maturation in the polychaete Hydroides elegans. Marine Ecology Progress Series, 168, 127134.
  • Skaer H.L.B. (1964) The water balance of a serpulid polychaete, Mercierella enigmatica (Fauvel) 1. Osmotic concentration and volume regulation. Journal of Experimental Biology, 60, 321330.
  • Smith E.B., Scott K.M., Nix E.R., Korte C., Fisher C.R. (2000) Growth and condition of seep mussels (Bathymodiolus childressi) at a Gulf of Mexico Brine Pool. Ecology, 81(9), 23922403.
  • Squires R.L., Goedert J.L. (1996) A new species of Thalassonerita? (Gastropoda: Neritidae) from a Middle Eocene cold-seep carbonate in the Humptulips formation, western Washington. Veliger, 39, 27272.
  • Tait N.N., Atapattu D., Browne R. (1981) Field and laboratory studies on salinity tolerance and osmotic behaviour in the polychaete Galeolaria caespitosa (Serpulidae). Australian Journal of Marine and Freshwater Research, 32, 769774.
  • Taviani M. (1994) The ‘‘calcari a Lucina’’ macrofauna reconsidered: deep-sea faunal oases from Miocene-age cold vents in the Romagna Appennine, Italy. Geo-Marine Letters, 14, 185191.
  • UNESCO (United Nations Educational, Scientific and Cultural Organization) (1985) The International System of Units (SI) in Oceanography. Report of IAPSO working group on symbols, units and nomenclature in physical oceanography (SUN). IAPSO Publication Scientifique, no. 32, UNESCO technical papers in marine science, no. 45.
  • Wolcott T.G. (1973) Physiological ecology and intertidal zonation in limpets (Acmaea): a critical look at ‘‘limiting’’ factors. Biological Bulletin, 145, 389432.
  • Zande J.M., Carney R.S. (2001) Population size structure and feeding biology of Bathynerita naticoidea Clarke 1989 (Gastropoda: Neritacea) from Gulf of Mexico hydrocarbon seeps. Gulf of Mexico Science, 2001(2), 107118.