The hypoxic tolerance of the protobranch bivalve Nucula sulcata bronn.ABSTRACT Examination of the hypoxic hypoxic a state of hypoxia. hypoxic cell sensitizers compounds that selectively sensitize hypoxic tumor cells to the effects of radiation. tolerance of Nucula sulcata determined that the mean survival time under hypoxia hypoxia Condition in which tissues are starved of oxygen. The extreme is anoxia (absence of oxygen). There are four types: hypoxemic, from low blood oxygen content (e.g., in altitude sickness); anemic, from low blood oxygen-carrying capacity (e.g. was 9.57 d with a maximum longevity of 30 d. Comparison between the three species, N. sulcata, N. nitidosa, and N. nucleus reveals that N. sulcata is the most tolerant of hypoxia followed by N. nucleus and N. nitidosa. It is suggested that the hypoxic tolerance of the species is a reflection of the normal habitat they occupy. KEY WORDS: environmental tolerance, hypoxia, Nucula sulcata, protobranch, adaptation INTRODUCTION The protobranch bivalves, Nucula sulcata, N. nucleus, and N. nitidosa are three of the five species of Nuculidae commonly found in soft sediments in British waters. Their distribution has been linked to particular sediment types, with IV. nitidosa inhabiting muddy sand; N. nucleus, muddy gravels; and N. sulcata sandy mud/mud, hence in most locations only one of the species is found. This has led to the suggestion that the distribution of the species is determined, in part, by their physiology. For example, N. nitidosa and N. nucleus have been shown to have different metabolic rates, which can be related to their particular habitats (Holmes et al. 2002, see also Wilson & Davies 1984, Creutzberg 1986). One important adaptation between the three species, that may affect their distribution, is their tolerance to hypoxia. With regard to N. nitidosa and N. nucleus, it has been determined that N. nucleus has a hypoxic tolerance ~3 times that of N. nitidosa, which may be reflected in its occupation of muddier habitats and hence an increase in its likelihood of experiencing hypoxic events (Holmes et al. 2002). The only observation pertaining per·tain intr.v. per·tained, per·tain·ing, per·tains 1. To have reference; relate: evidence that pertains to the accident. 2. to the hypoxic tolerance of N. sulcata is effectively anecdotal in nature (Taylor et al. 1995) with no replication and/or independence of experimental design, as is the case for most hypoxic tolerance studies (see Dries & Theede 1974 and Zwaan et al. 2001 for examples). The aim of this study, was to measure the hypoxic tolerance of N. sulcata, using an experimentally robust design and directly compare these results with those obtained for N. nitidosa and N. nucleus in earlier years, previously published elsewhere (Holmes et al. 2002), under the hypothesis that the hypoxic tolerance of the species should increase as the mud content of their habitat increases (i.e. as the likelihood of the frequency of hypoxic events increases). MATERIALS AND METHODS Bivalves, N. sulcata, were collected in the mouth of Gullmarsfjord, off Gaso island (58[degrees]14.19'E 11[degrees]26.36'N) in 2001, using an Agassiz trawl trawl - To sift through large volumes of data (e.g. Usenet postings, FTP archives, or the Jargon File) looking for something of interest. , and taken to Kristineberg Marine Research Station, Fiskerbackskil, Sweden where all experiments were carried out. Once at the laboratory, the specimens were left for 5 days in sediment to acclimatize, in running seawater seawater Water that makes up the oceans and seas. Seawater is a complex mixture of 96.5% water, 2.5% salts, and small amounts of other substances. Much of the world's magnesium is recovered from seawater, as are large quantities of bromine. (~10[degrees]C). Measurement of the hypoxic tolerance of N. sulcata was made as follows (the measurement of the hypoxic tolerance of IV. nitidosa and N. nucleus was made in an identical fashion and is reported elsewhere [Holmes et al., 2002]). Ten liters of autoclaved filtered (0.2 [micro]m) seawater (10[degrees]C) was vigorously bubbled with filtered (0.2 [micro]m) [N.sub.2], in a semi-enclosed vessel, for 6 h prior to the start of the experiment (i.e., to ensure that the seawater contained as little oxygen as possible). One hundred and twenty, 9-mL (nominal) bottles were then filled with the seawater and a randomly selected animal placed into each. Ninety of the bottles were then capped, ensuring that the bottle remained under the surface of the water at all times (treatment animals), and the remaining 30 bottles were left uncapped (control animals). In addition, 35 bottles were filled with seawater and the bottles capped (water control). Five of these bottles were immediately analyzed for their oxygen content (Holmes et al. 2002). All of the bottles were placed together under a 12 h day/night cycle and maintained at 10[degrees]C for the duration of the experiment. Every day, the treatment and control animals were inspected, individually, to ascertain whether they were alive. If an animal was found to be dead, it was removed from the experiment and its death recorded along with its shell height, width, length, whole dry weight, flesh dry weight, and the oxygen concentration of the water. Every 5 days, from the start of the experiment, 5 randomly selected water controls were removed and the oxygen concentration determined. The end of the experiment was determined by the death of all of the animals. It should be noted that, the measurements of hypoxic tolerance made here will inherently include other confounding confounding when the effects of two, or more, processes on results cannot be separated, the results are said to be confounded, a cause of bias in disease studies. confounding factor factors (e.g., starvation) that will result in an under, rather than over estimation. RESULTS AND DISCUSSION The mean oxygen concentration of the seawater at the start of the experiment [+ or -] standard error (SE) was 1.56 [+ or -] 0.13 mL [O.sub.2] [1.sup.-1] and hence the seawater can be regarded as hypoxic at the start of the experiment, see Figure 1 (Diaz & Rosenberg 1995). Comparison of the control water oxygen concentration during the experiment, using ANOVA anova see analysis of variance. ANOVA Analysis of variance, see there , revealed no differences. Linear regression Linear regression A statistical technique for fitting a straight line to a set of data points. of the lifetime of N. sulcata versus the mean oxygen concentration of the water samples, at the time of death, produced a statistically significant regression. The [O.sub.2] concentration of the water for the treatment animals dropped over time as they respired, leading to their eventual death (Fig. 1). Analysis of the number of animals dying per day, against the mean [O.sub.2] concentration for the animals that died that day, using Spearman's rho Spearman's rho, n.pr a statistical test for correlation between two rank-ordered scales. It yields a statement of the degree of interdependence of the scores of the two scales. , to determine if there was a threshold [O.sub.2] concentration lower than that at the start of the experiment that caused death, produced no statistically significant correlation; the initial [O.sub.2] concentration of the water was sufficient without any further reduction in its oxygen concentration to cause death by hypoxia. Correlation, using Spearman's rho, of the shell length, height, width, whole body dry weight, and dry flesh weight data to the survival data, failed to produce any statistically significant correlations (i.e. death caused by hypoxia does not seem to be related to body size). [FIGURE 1 OMITTED] Analysis of the survival data, using the Kaplan-Meier procedure with log rank comparisons (Klein & Moeschberger 1998), determined that survival rate of the N. sulcata treatment animals was different from that of the N. sulcata control animals (P = 0.003, Fig. 2). The mean [+ or -] SE survival time for the treatment animals was 9.57 [+ or -] 0.68 d (median = 7 d, [LT.sub.50] = 7 d) and 14.45 [+ or -] 1.27 d (median = 13 d, [LT.sub.50] = 13 d) for the control animals (Fig. 2). For the treatment and control animal the maximum longevity was 30 d. Note, 13 treatment animals and one control animal bottles were broken during the experimental period and hence were excluded from the analysis. Comparison between the previously published survival data for N. nitidosa and N. nucleus with the N. sulcata data, again using the Kaplan-Meier procedure with log rank comparisons, revealed that survival rates for all species were different from each other (P [less than or equal to] 0.003) (Fig. 2). That is, N. nitidosa (mean [+ or -] SE survival time = 3.53 [+ or -] 0.28 d) was most susceptible to death by hypoxia followed by N. nucleus (mean [+ or -] SE survival time = 7.72 [+ or-] 0.21 d) and then by N. sulcata. In effect, N. sulcata has a hypoxic tolerance ~1.25 times greater than that of N. nucleus and 5 times that of N. nitidosa. In terms, of total longevity (i.e., the time taken for all animals to die), N. sulcata has a maximum longevity of approximately twice that of N. nucleus (longevity ~15 d) and approximately three times that of N. nitidosa. The maximum survival time recorded for N. sulcata (30 d) is less than that recorded, but of the same order, for Corbula gibba (34 + d), which occupies a similar habitat (Holmes & Miller 2006). [FIGURE 2 OMITTED] With regard to the existing observation within the literature as to the hypoxic tolerance of N. sulcata ([LT.sub.50] = 14 d and longevity = 21 d) (Taylor et al. 1995) the values reported here are different. In part, arising from the different methodologies used but also from the more robust experimental design adopted. Irrespective of irrespective of prep. Without consideration of; regardless of. irrespective of preposition despite the cause of the difference, the results presented here for N. sulcata are directly comparable with those recorded for N. nitidosa and N. nucleus, revealing as hypothesized that the hypoxic tolerance of the three species can be linked to the habitat they normally occupy. In terms of comparison with other nuculides, N. tenuis ten·u·is n. pl. ten·u·es Linguistics 1. A voiceless stop. 2. A voiceless unaspirated stop in ancient Greek. has been recorded as having a maximal longevity of 17 d (Moore 1931), and there are no observations for N. hanleyi. If the hypothesis substantiated were correct, then it would be interesting to measure the hypoxic tolerance of N. hanleyi, which should be approximately equal to or lower than that of N. nitidosa and N. hanleyi occupying sandy sediments with a high oxygen concentration. Similarly, the hypothesis could be expanded to a range of bivalve bivalve, aquatic mollusk of the class Pelecypoda ("hatchet-foot") or Bivalvia, with a laterally compressed body and a shell consisting of two valves, or movable pieces, hinged by an elastic ligament. species, for example Abra alba, which inhabits sandy mud and has a much lower hypoxic tolerance than A. elliptica occupying muddy/gravely sands (Dries & Theede 1974). The importance in individual, nonobservable, adaptations between closely related species in determining their distribution patterns has been often overlooked in sublittoral sub·lit·to·ral adj. 1. a. Of or situated near the seashore. b. Of or relating to an organism living near or just below the low tide level of a shore. 2. benthic ben·thos n. 1. The collection of organisms living on or in sea or lake bottoms. 2. The bottom of a sea or lake. [Greek. ecology. However, any experiments performed to attempt to discern adaptational differences need to be done in an experimentally robust manner, with independent observations, such that correct cross comparisons between species can be attained. LITERATURE CITED Creutzberg, F. 1986. Distribution patterns of two bivalve species (Nucula turgida and Tellina fabula) along a frontal system in the Southern North Sea. Neth. J. Sea Res. 20:305-311. Diaz, R. J. & R. Rosenberg. 1995. Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of macrobenthic fauna. Oceanogr. Mar. Biol. Ann. Review 33:245-303. Dries, R. R. & H. Theede. 1974. Resistance to oxygen deficiency in marine bottom invertebrates of the Western Baltic Sea Baltic Sea, arm of the Atlantic Ocean, c.163,000 sq mi (422,170 sq km), including the Kattegat strait, its northwestern extension. The Øresund, Store Bælt, and Lille Bælt connect the Baltic Sea with the Kattegat and Skagerrak straits, which lead to the . Mar. Biol. 25:327-333. Holmes, S. P. & N. Miller. 2006. Aspects of the population genetics Population genetics The study of both experimental and theoretical consequences of mendelian heredity on the population level, in contradistinction to classical genetics which deals with the offspring of specified parents on the familial level. and ecology of the bivalve Corbula gibba. Mar. Ecol. Prog. Ser. 315:129-140. Holmes, S. P., N. Miller & A. Weber. 2002. The respiration respiration, process by which an organism exchanges gases with its environment. The term now refers to the overall process by which oxygen is abstracted from air and is transported to the cells for the oxidation of organic molecules while carbon dioxide (CO and hypoxic tolerance of Nucula nitidosa and N. nucleus: factors responsible for determining their distribution? J. Mar. Biol. Assoc. UK. 82:971-981. Klein, J. P. & M. L. Moeschberger. 1998. Survival analysis-techniques for censored cen·sor n. 1. A person authorized to examine books, films, or other material and to remove or suppress what is considered morally, politically, or otherwise objectionable. 2. and truncated data. New York New York, state, United States New York, Middle Atlantic state of the United States. It is bordered by Vermont, Massachusetts, Connecticut, and the Atlantic Ocean (E), New Jersey and Pennsylvania (S), Lakes Erie and Ontario and the Canadian province of : Springer-Verlag. Moore, H. B. 1931. The muds of the Clyde Sea area. III. Chemical and physical conditions; rate and nature of sedimentation sedimentation In geology, the process of deposition of a solid material from a state of suspension or solution in a fluid (usually air or water). Broadly defined it also includes deposits from glacial ice and materials collected under the effect of gravity alone, as in talus and fauna. J. Mar. Biol. Assoc. UK. 17:325-358. Taylor, C., J. Davenport & J. A. Allen. 1995. Anoxic an·ox·i·a n. 1. Absence of oxygen. 2. A pathological deficiency of oxygen, especially hypoxia. [an- + ox(o)- + -ia1. survival, oxygen consumption and haemocyanin Haem`o`cy´a`nin n. 1. Same as Hæmacyanin. characteristics in the protobranch bivalve Nucula sulcata Bronn. Comp. Biochem. Physiol. 112:333-338. Wilson, J. G. & J. P. Davies. 1984. The effects of environmental variables on the oxygen consumption of the protobranch bivalve Nucula turgida (Leckenby and Marshall). J. Moll. Stud. 50:73-77. Zwaan, A., O. Cattani, G. Vitali & P. Cortesi. 2001. Influence of incubation conditions on the anoxic survival of marine bivalves: static and semi-static incubations. Mar. Ecol. Prog. Ser. 211:169-179. SEBASTIAN P. HOLMES (1,2) AND NICOLA MILLER (1) (1) Port Erin Coordinates: Port Erin (Manx: Purt Chiarn) is a town in the south of the Isle of Man. Its population is 3,369 according to the 2001 census. The name means either Lord's Port or Iron Port. Marine Laboratory, Port Erin, Isle of Man Noun 1. Isle of Man - one of the British Isles in the Irish Sea Man British Isles - Great Britain and Ireland and adjacent islands in the north Atlantic , IM9 6JA, British Isles British Isles: see Great Britain; Ireland. , (2) The Ministry of Fisheries Many states have set up government departments, usually called ministries, which regulate fisheries management within the state's exclusive economic zone. Examples include:
* Corresponding author. E-mail: s.p.holmes@liverpool.ac.uk |
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