The physiological condition of the hydrothermal vent mussel, Bathymodiolus thermophilus at two sites on the East Pacific Rise
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1 The physiological condition of the hydrothermal vent mussel, Bathymodiolus thermophilus at two sites on the East Pacific Rise Joanne E. Glanville The Pennsylvania State University Mentors: Breea Govenar and Dr. Charles Fisher Department of Biology, The Pennsylvania State University Abstract A total of five collections were made of the mussel Bathymodiolus thermophilus at two sites in the East Pacific Rise, Mussel Bed and Biovent. Four collections were made during three different dives at Mussel Bed and one collection was made during one dive at Biovent. The soft tissue was weighed at sea, dried in lab and weighed again; the mussel shells were dried and their length and volume was recorded; the number of Branchipolynoe symmytilida present in each mussel was also recorded. The condition index (soft tissue dry mass / total shell volume) of the mussels was calculated in lab along with all other statistics. There was no significant difference between the condition indices of the mussels from the two sites. However, it was also observed that the presence of two polynoid polychaetes inside the mussels was correlated with a significantly lower condition index of the mussels at both sites. Introduction Hydrothermal vents were first discovered at the Galapagos Rift in the eastern Pacific Ocean in These hot springs, which exist approximately 2.5 km from the surface, are found at the sea floor spreading centers (Childress et al. 1987). Warm water, containing hydrogen sulfide and other chemicals, seeps through fractures on the ocean floor and sustains invertebrate communities at the hydrothermal vent sites. Free living and symbiotic chemoautotrophic bacteria oxidize the hydrogen sulfide to generate organic compounds, which serve as the base of the food web. Each vent site is characterized by its own unique mixture of fauna that varies in the density and diversity of species. On the East Pacific Rise (9 o 50 N, 104 o 20 W) masses of long Riftia pachyptila tube worms with brightly colored plumes visually dominate active venting areas. Giant clams, Calyptogena magnifica, occur in areas of low diffuse flow (Childress et al. 1987). The mussel Bathymodiolus thermophilus can be found with R. pachyptila or C. magnifica in a variety of microhabitats (Fisher et al. 1988, Gage & Tyler 1999). Aggregations of B. thermophilus are found in a wide range of environmental conditions at the East Pacific Rise. Mussels may occur with tube worms in areas of active hydrothermal flow, where the temperature and the concentration of hydrogen sulfide is higher; and with clams in areas of diffuse hydrothermal flow, where the temperature and the concentration of hydrogen sulfide is lower (Van Dover 2000). Studies have shown
2 that B. thermophilus can quickly adapt to a wide range of environmental conditions (Smith 1985), and thus these mussels are usually the last survivors in a hydrothermal vent field where there is no longer any active venting (Van Dover 2000). Mussels from sites that are near active hydrothermal flow have a healthier physiological condition than mussels that are either further away from venting areas or that are in locations where the venting has decreased (Fisher et al. 1988). B. thermophilus has the ability to live in a variety of vent microhabitats because it contains sulfur-oxidizing endosymbiotic bacteria and can also filter feed on particulates. Even though the symbiotic mode of nutrition has been verified by enzyme assays (RuBP carboxylase, ATP sulfurylase and APS reductase) and stable isotopic analyses, the primary source of the nutrition is not clear, because the mussels have a complete digestive tract and show evidence of filter-feeding (Fisher et al. 1988, Fisher et al. 1994, Nelson et al. 1994). Mussel populations undergo a natural biological succession where their length and tissue dry weight increases as the individuals get older, and finally die off along with diminishing hydrothermal vent activity (Van Dover 2002). The ratio of tissue dry weight to total shell volume (condition index) is calculated in order to determine a relative index of the physiological condition of the mussels. In some mussels, a commensal polynoid polychaete, Branchipolynoe symmytilida is found in the mantle cavity. Fisher et al. (1994) found stable isotopic evidence that these polynoid worms obtain a significant proportion of their nutrition from their mussel hosts, apparently feeding on pseudofaeces, mucous, or gill tissue. In this study we are comparing the physiological condition of mussels from two sites at the East Pacific Rise (EPR); Mussel Bed (MB) and Biovent (BV). Specifically we compare the condition index (dry weight of soft tissue/ total volume of shell), size (dry weight of soft tissue biomass, length of shell), and the presence and abundance of the polynoid, B. symmytilida. Methodology Site description and sample collection: Five collections of the hydrothermal vent mussel, Bathymodiolus thermophilus, were sampled from two hydrothermal vent sites at the East Pacific Rise in December Mussel Bed ( N, W) and Biovent ( N, W) lay approximately 200 m apart from each other along the Axial Summit Caldera. The submersible Alvin was used on three dives at the Mussel Bed site (A3741, A3736, A3729) and one dive at the Biovent site (A3739). A sampling device named the ChimneyMaster (diameter: 30cm) was used for two collections in dive A3729 and one collection each on dives A3739 and A3736. For the A3741 dive a different sampling device named the BushMaster (diameter: 60cm) was used to make one collection. All the collections were documented on digital video at the time of sampling. On board the ship, the seawater was drained from the mussels and the number of B. symmytilida found inside the mantle cavity of the mussels was recorded. The soft tissue was removed, weighed using a motion compensated shipboard balance, and frozen in pre-weighed bags
3 to be transported back to the laboratory to determine the dry weight of the tissue. The shells of the mussels were measured for length, cleaned, and brought back to the laboratory to measure the internal volume. Condition index of mussels: The condition index of the mussels was determined as: CI = (soft tissue dry mass) (internal shell volume) (Smith 1985, Fisher et al. 1988). In the lab, the frozen soft tissue was thawed and dried at 60 o C. The dried tissue was weighed every 24 hours until the difference between consecutive weights was less than 5%. To determine the shell volume, both valves of the mussel were filled with sand and weighed. Each valve was measured for every individual mussel for all the collections. Fixed volumes of sand (10, 35, 75, and 100 cm 3 ) were weighed three times on a metric balance to construct a calibration curve and convert the volume of sand to mass. The mass of the shells was multiplied by the conversion factor of sand volume to mass (g/cm 3 ) to calculate the volume of the shell. Statistical analyses: The statistical software program Minitab 12 for Windows was used to construct a general linear model and calculate the analysis of variance (ANOVA) for three response variables: condition index, dry weight, and shell length. In each model, three predictor variables were used: collection, site, and presence of B. symmytilida. Pairwise comparisons of the factor level response values were made with the Bonferroni procedure (α = 0.05). A Student s t-test was also used to test the significance of the difference between the two sites, Mussel Bed and Biovent, with three variables: condition index, dry weight, and shell length. Results Condition index of B. thermophilus: Results of the analysis of variance model indicate that the collection (ANOVA: α = 0.05; p = 0.046) and presence of B. symmytilida (ANOVA: α = 0.05; p = 0.029) significantly affect the condition index of the mussels at both sites. However, after the Bonferroni correction for multiple comparisons, the differences between the condition indices of the mussels from different collections are not significant. The condition index of the mussels with two B. symmytilida is significantly lower than mussels with one or zero polynoids for all collections (Student s t: α = 0.05; µ 0 µ 2, p = 0.026; µ 1 µ 2, p = 0.027). A Student s t-test demonstrated no significant difference (Student s t: α = 0.05; p = 0.95; Table 1) between the condition index of the mussels collected from the two sites, Mussel Bed and Biovent (Fig. 1). Shell length and dry weight of mussel tissue: In the analysis of variance models of the two size parameters (tissue dry weight and shell length), none of the predictor variables (collection, site, and the presence of B. symmytilida) significantly affected the dry weight of the mussels; but the collection does significantly affect the length of the mussel shells (ANOVA: α = 0.05; p = 0.004).
4 Although, with the Bonferonni correction for multiple comparisons, no significant differences are detected between the shell lengths in all five collections, the Student s t- test reveals (Figs. 2 and 3) that the mussels collected at Biovent had a higher average shell length and tissue dry weight than the mussels collected at Mussel Bed (Student s t: α = 0.05; shell length, µ BV µ MB, p = 0.001, dry weight, µ BV µ MB, p = ; Table 1). Presence of Branchipolynoe symmytilida: As many as two B. symmytilida were found in the mantle cavity of an individual mussel, but in most of the mussels there was only one or none at all. For both sites, it has been demonstrated that the condition index was significantly lower (Figs. 4 and 5) when two B. symmytilida were present in the mussels (ANOVA, α = 0.05: µ 0 µ 2, p = ; µ 1 µ 2, p = ). The condition index was not significantly lower with the presence of only one polychaete (ANOVA, p = ). Discussion The mussels collected at Biovent and Mussel Bed have very similar condition indices. This could be either because the collection sites have similar environments, or because the mussels adapt quickly to their environment and therefore can be equally healthy in two different microhabitats. Upon closer inspection, the mussels at Biovent have, on average, greater shell length and a higher tissue dry weight than the mussels collected from Mussel Bed. Thus, the mussels at Biovent could be older or in a later biological succession stage than the mussels at Mussel Bed. The size differences more likely reflect age, rather than environmental differences, because the condition indices are not significantly different at the two sites. Fisher et al. (1994) suggested that the polynoid B. symmytilida obtains its nutrition by eating mucous and pseudofaeces from the mussels. In all collections, the average condition index was significantly lower when two polynoids were present in the mussel. This might suggest that the polynoid might have a negative impact on the mussel by damaging or eating the tissue, or that the worms are choosing to inhabit the mussels that have a lower condition index The percent of mussels containing B. symmytilida for each site was also calculated. According to the calculations Biovent mussels had a higher presence of the polychaete than the mussels at Mussel Bed (BV=75%, MB=48%). A factor that might influence the greater frequency of B. symmytilida in the mussels at Biovent is the possibility of fewer predators than occur at Mussel Bed, as suggested by Fisher et al in different sites at the Galapagos Rift. However, the relative number of mussels found with polynoids at the two sites, may be biased because of the small sample size (N BV = 12, N MB = 70) and so more extensive sampling would be needed to further test these observations. Conclusion Hydrothermal vent mussels have the ability to live in a variety of microhabitats. Previous studies have shown that the physiological condition of B. thermophilus is strongly affected by environmental conditions. A good estimate of the physiological condition of mussels in different habitats is the condition index. In this study, samples taken from two different hydrothermal vent sites do not show significantly different condition indices
5 between sites. However, the significant size differences between the mussels at Biovent and Mussel Bed may represent two different colonization events. Larger mussels with relatively the same proportion of soft tissue biomass as smaller mussels could be older or in a more advanced biological successional stage. At both sites, the condition index of the mussels that contained two B. symmytilida was significantly lower than the condition index of the mussels that contained one or no polynoids, in all collections. This may suggest that the relationship with B. symmytilida may be parasitic, when there are more than one polynoid in an individual mussel. Future research on the physiological condition of B. thermophilus at different hydrothermal vent habitats may also consider the relationship of the symbiotic polynoid, B. symmytilida.
6 Condition index (g/cm3) Sites MB BV Fig. 1. The average condition index (g/cm 3 ) of the mussels collected at each site. There is no significant difference between the condition indices of the mussels at Mussel Bed (MB) and Biovent (BV), p = 0.95.
7 Average dry weight (g)/ individual Sites MB BV Fig. 2. The average shell length (cm) of the mussels collected at each site. The average shell length (cm) of the mussels from Biovent (BV) is significantly larger than Mussel Bed (MB), p = Average length (cm)/ individual Sites MB BV Fig. 3. The average dry tissue weight (g) of the mussels collected at Biovent (BV) is significantly larger than the mussels collected at Mussel Bed (MB), p =
8 Average condition index (g/cm3) Number of B. symmytilida present Fig. 4. There is a negative correlation between the average condition index (g/cm 3 ) and the increasing number of B. symmytilida found in the mantle cavity of the mussels at Mussel Bed (MB). Average condition index (g/cm3) Number of B. symmytilida present Fig. 5. There is a negative correlation between the average condition index (g/cm 3 ) and the increasing number of B. symmytilida found in the mantle cavity of the mussels at Biovent (BV).
9 Collection Site N Condition index (g/cm 3 ) Dry weight (g) Shell length (cm) A3729 MB (0.016) (1.681) (15.69) A3736-CM1 MB (0.011) (2.281) (24.24) A3736-CM2 MB (0.025) (2.370) (31.05) A3739 BV (0.023) (4.97) (18.99) A3741 MB (0.023) (2.473) (29.83) Table 1. Number of mussels collected during each dive along with the average (standard deviation) of the condition index, tissue dry weight, and shell lengths for all of the mussel collections.
10 References Childress J. J., H. Felbeck and G. N. Somero (1987) Symbiosis in the Deep Sea. Scientific American, Vol. 256, pp Fisher C. R., J. J. Childress, A. J. Arp, J. M. Brooks, D. Distel, J. A. Favuzzi, H. Felbeck, R. Hessler, K. S. Johnson, M. C. Kennicutt II, S. A. Macko, A. Newton, M. A. Powell, G. N. Somero and T. Soto (1988) Microhabitat variation in the hydrothermal vent mussel, Bathymodiolus thermophilus, at the Rose Garden vent on the Galapagos Rift. Deep-Sea Research, Vol. 35, pp Fisher C. R., J. J. Childress, S. A. Macko, J. M. Brooks (1994) Nutritional interactions in Galapagos Rift hydrothermal vent communities: inferences from stable carbon and nitrogen isotope analyses. Marine Ecology Progress Series, Vol. 103, pp Gage J. D. and P. A. Tyler (1999) Deep-Sea biology: A Natural History of Organisms at the Deep-Sea floor, Cambridge University Press, Cambridge, pp Nelson D. C., K. D. Hagen and D. B. Edwards (1995) The gill symbiont of the hydrothermal vent mussel Bathymodiolus thermophilus is a psychrophilic, chemoautotrophic, sulfur bacterium. Marine Biology, Vol. 121, pp Smith K. L. Jr. (1985a) Deep-Sea hydrothermal vent mussels: Nutritional state and distribution at the Galapagos Rift. Ecology, Vol. 66, pp Van Dover C. L. (2000) The Ecology of Deep-Sea Hydrothermal Vents, Princeton University Press, New Jersey, pp Van Dover C. L. (2002) Community structure of mussel beds at deep-sea hydrothermal vents. Marine Ecology Progress Series, Vol. 230, pp
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