Body oxygen stores, aerobic dive limits and diving behaviour of the star-nosed mole (Condylura cristata) and comparisons with non-aquatic talpids
Department of Zoology, University of Manitoba, Winnipeg, Manitoba, Canada R3T 2N2
*Author for correspondence (e-mail: rmacarth{at}ms.umanitoba.ca)
Accepted 18 October 2001
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Summary |
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Key words: aerobic dive limit, body oxygen store, diving behaviour, energetics, myoglobin, insectivore, star-nosed mole, Condylura cristata, coast mole, Scapanus orarius, lung volume.
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Introduction |
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One such animal is the star-nosed mole Condylura cristata. Of the seven species of North-American moles (Family Talpidae), only the star-nosed mole is semi-aquatic. This accomplished diver frequents tunnel systems excavated along the edges of streambeds and lakes and relies on aquatic insects and annelids for a substantial proportion of its diet (Hamilton, 1931; Rust, 1966
). Despite its small size and presumed susceptibility to immersion hypothermia (MacArthur, 1989
), this insectivore is reported to forage actively in near-freezing water during the frigid winter months (Merriam, 1884
; Hamilton, 1931
). In a preliminary study of the diving behaviour of six star-nosed moles, we observed dive durations that greatly exceeded predictions based on allometric theory (Schreer and Kovacs, 1997
). The average dive times of these moles rivalled those of the mink (Dunstone and OConnor, 1979
), a semi-aquatic mustelid that is approximately 20 times larger than Condylura cristata. Given its small mass and inherently high basal metabolic rate, BMR (twice the mass-predicted value) (Campbell et al., 1999
), and hence potentially high rate of O2 utilization under water, the star-nosed mole presents an intriguing model for investigating mammalian dive endurance.
The purpose of this study was threefold. First, we wished to determine the extent of total body O2 stores and estimate the diving metabolic rate (DMR) of star-nosed moles in order to derive the theoretical aerobic dive limit (ADL) of this species. A second goal was to assess the correspondence, if any, between the calculated ADL and behavioural indices of the dive performance of star-nosed moles. Our final objective was to compare the oxygen storage capacity and potential for anaerobic metabolism in two talpids of similar mass and phylogenetic history: the semi-aquatic star-nosed mole and the strictly fossorial coast mole Scapanus orarius.
This comparison is relevant because both species are specialized for burrowing, and it is useful to know the extent to which diving has modified respiratory functions in the star-nosed mole. Since respiratory specializations for diving are potentially convergent with patterns seen in fossorial species, we hope that this study will shed light on the general mechanisms underlying hypoxia-tolerance in talpids. For example, previous studies have consistently demonstrated high muscle myoglobin (Mb) concentrations in divers (see Kooyman and Ponganis, 1998) and in non-diving, burrowing mammals such as the echidna Tachyglossus aculeatus (Hochachka et al., 1984
) and the mole rat Spalax ehrenbergi (Widmer et al., 1997
). It is conceivable that fossorial moles also exhibit enhanced oxygen stores, possibly to compensate for the low ambient O2 tensions prevalent in closed-burrow systems (Schaefer and Sadleir, 1979
). Are the tissue oxygen stores of star-nosed moles further enhanced by a dependence on diving? In addition to comparing the partitioning of body oxygen reserves, we assessed the potential for anaerobic metabolism from measurements of buffering capacity in the fore- and hindlimb muscles of the two mole species.
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Materials and methods |
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In May 1999, 11 adult coast moles (Scapanus orarius True) were live-trapped near Abbottsford, British Columbia, Canada, and immediately transported to the Department of Zoology, University of British Columbia. Holding conditions were identical to those adopted for the star-nosed mole, with the exception that coast moles were housed in large soil-filled plastic containers (46 cmx33 cmx38 cm) with no provision for swimming. The frozen carcasses of 11 additional coast moles were provided by a local mole trapper for muscle mass determinations. Muscle samples from two American shrew moles Neurotrichus gibbsii Baird, obtained as part of another, unrelated study (K. L. Campbell, unpublished data), were also analyzed for Mb content (see below). This study complied with University of Manitoba and University of British Columbia regulations governing animal research and at all times animals were cared for in strict accordance with Canadian Council on Animal Care guidelines.
Diving behaviour
Following 3 weeks acclimation to the animal holding facilities, 18 star-nosed moles were used in a study of voluntary diving behaviour. Dive trials were performed in a large fibreglass-lined plywood tank fitted with removable wooden and Plexiglas panels. The tank was provided with a dry resting platform (17.5 cmx68 cm), and the swimming/diving section (180 cmx68 cmx72 cm) was covered by a Plexiglas sheet except for an open swimming area immediately adjacent to the platform. The tank was filled to a depth of 61 cm with water at 3, 10, 20 or 30°C. Of the 18 moles tested, only seven were exposed to all four water temperatures. For these individuals, trials were conducted in random order and on separate days. At the start of each 20 min trial, the mole was released onto the dry resting platform and allowed to move freely throughout the tank. The durations and frequencies of all diving, swimming, resting and grooming episodes were recorded on audiotape for subsequent analyses.
Diving respirometry
To estimate the metabolic cost of diving, a series of diving trials was conducted in a covered fibreglass tank (208 cmx55 cmx52 cm) filled to a depth of 44 cm with water. The animal was prevented from surfacing anywhere in the tank except in a 2.6 l Plexiglas metabolic chamber mounted on the Plexiglas tank cover. The chamber was similar in design to a larger version constructed for muskrats (MacArthur and Krause, 1989). Air entered the chamber via a series of small holes bored in one of the walls near water level and was drawn by vacuum through the chamber via a ceiling exhaust port located at the opposite side of the structure. Gas mixing was facilitated by an electric fan installed in the chamber ceiling (MacArthur and Krause, 1989
). The flow rate was maintained at 940 ml min1 using a combination pump/mass flow meter (TR-SS1 gas analysis subsampler; Sable Systems Inc., Henderson, NV, USA). Excurrent air was drawn sequentially through a column of soda lime and a column of Drierite to eliminate CO2 and H2O vapour, respectively. A 250 ml sub-sample of dry, CO2-free exhaust gas was drawn through the M-22 sensor of an Applied Electrochemistry S3-A oxygen analyser for determination of the fractional oxygen content of expired gas, FEO2 (resolution 0.01 %). Air flow rate through the metabolic chamber (ml min1), FEO2 and water temperature (°C) were recorded every 5 s using a Sable Systems Universal Interface and Datacan V data-acquisition software (Sable Systems Inc.).
Pretrial training sessions were conducted to familiarize animals with the diving tank and metabolic chamber. During training, the length of the tank available for diving was varied using removable Plexiglas partitions. Training runs were performed at an initial tank length of 90 cm, which was subsequently extended to 144 cm and, finally, to 191 cm. Prior to each trial, the water level was adjusted to the prescribed depth to ensure a constant gas volume in the metabolic chamber; water temperature was maintained at 30±0.5°C. At this temperature, star-nosed moles exhibited maximal diving activity in the 20 min behavioural trials described above and were presumably under minimal thermal stress. Moles were weighed to the nearest 0.01 g approximately 10 min before the start of each trial.
In 1997, the duration of metabolic trials in water was limited to 8 min. However, as our preliminary findings indicated that the proportion of time spent diving increased with trial duration, aquatic trials were extended to 10 min in 1999. Animals gained access to the tank and metabolic chamber via a hinged door mounted on the tank cover. Both diving behaviour and activity in the metabolic chamber were closely monitored and recorded on a Sony tape recorder. Upon completion of the trial, a plunger mounted in the ceiling of the metabolic chamber was gently depressed, prompting eviction of the animal without interrupting gas analysis. This step facilitated measurement of the total oxygen consumed over a constant period of immersion (MacArthur and Krause, 1989). The animal was then permitted to leave the water and enter a dry nest box, at which point it was transferred to a large container of soil. All animals were fed immediately prior to metabolic testing. The mean rate of oxygen consumption (
O2) was calculated for the entire run following equation 4a in Withers (1977
). This value represents the combined costs of diving and surface swimming by the mole during the 8- or 10-min test period in water. For the purpose of calculating the ADL (see below), this mean
O2 was assumed to approximate DMR. In most cases, moles swam continuously during each trial, alternating between diving and swimming at the surface. Unfortunately, given the short run time, we could not separate the costs of diving from those of surface swimming in these animals.
To obtain baseline metabolic measurements for intra- and interspecific comparisons, we measured the resting metabolic rate (RMR) of star-nosed moles at thermoneutrality in air. In this case, the metabolic chamber consisted of a modified 0.95 l paint can with a flat black interior that was fitted with inlet and outlet air ports and furnished with 34 mm of dry, sterilized soil. During each 1 h trial, the chamber was housed in a controlled-environment cabinet set at 30±0.5°C. The lowest O2 maintained over at least a 3 min period of inactivity was taken as the RMR. The absence of motor activity was verified independently using a motion activity detector (MAD-1; Sable Systems Inc.) mounted directly beneath the metabolic chamber. Otherwise, the procedure for determining the
O2 of resting animals in air was identical to that described for diving/swimming star-nosed moles.
Body oxygen stores
After completion of aquatic trials, 11 star-nosed moles were killed with an overdose of inhalant anaesthetic (Halothane; MTC Pharmaceuticals, Cambridge, Ontario, Canada) to assess the O2 storage capacities of the blood, lungs and skeletal muscles. While moles were deeply anaesthetized, a blood sample was drawn by cardiac puncture for haemoglobin (Hb) and haematocrit (Hct) determinations (MacArthur, 1984b).
To obtain sufficient tissue for analyses, the entire heart and as much forelimb and hindlimb muscle as possible were harvested from freshly killed animals and immediately frozen at 70°C. For all comparisons, care was taken to sample identical fore- and hindlimb muscles. Sub-samples (0.5 g) of pooled fore- or hindlimb muscles collected from each animal were subsequently analysed for Mb concentration following the procedure of Reynafarje (1963). Samples of skeletal muscle from coast moles and shrew moles were treated in an identical manner, with the exception that muscle from these species was freeze-clamped in liquid N2 prior to freezing at 70°C.
The lungs of star-nosed and coast moles were excised, and lung volume was determined gravimetrically (Weibel, 1970/71; MacArthur, 1990
). For this purpose, the lungs were immersed in saline (0.9 mol l1 NaCl) and inflated with humidified air at a constant pressure of 2.7 kPa. Final lung volume was corrected to standard temperature and pressure. Following removal of the internal organs, skin, eyes and brain, the eviscerated carcass was weighed, immersed in a detergent solution, and boiled for approximately 48 h to remove the remaining skeletal muscle. The mass of the dry skeleton was subsequently determined and subtracted from eviscerated carcass wet mass to derive total skeletal muscle mass.
The blood volumes (Vb; ml) of star-nosed and coast moles were estimated from the allometric equation:
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where M is body mass (kg) (Prothero, 1980). Otherwise, the calculation of lung, blood and muscle O2 stores followed conventional protocols (Lenfant et al., 1970
; Kooyman, 1989
; MacArthur et al., 2001
). For star-nosed moles, the theoretical or calculated ADL (s) was determined by dividing the total body oxygen stores (ml O2, STPD) by the mean swimming/diving
O2 (ml O2 s1) obtained for each animal. Implicit in these calculations is the assumption that all oxygen reserves are fully exploited under water (Kooyman, 1989
). We also determined the behavioural ADL, previously defined by Kooyman et al. (1983
) and Burns and Castellini (1996
) as the dive time exceeded by only 5 % of all voluntary dives.
Muscle buffering capacity
The buffering capacities of forelimb and hindlimb muscles were determined following the procedure of Castellini and Somero (1981). Briefly, a muscle sample (0.5 g) was homogenized in 0.9 mol l1 NaCl and then titrated at 37°C with 0.2 mol l1 NaOH. The pH of the homogenate was determined using a Corning model 360 pH meter equipped with an ISFET electrode. Buffering capacity, measured in slykes, is defined as the amount of base required to raise the pH of 1 g of wet muscle from 6 to 7 (Van Slyke, 1922
).
Statistical treatment of data
Two-sample comparisons of mean values were made using Students or Welchs t-test or one-way analysis of variance (ANOVA) where appropriate. For interspecific comparisons of muscle variables, a split-plot design was employed (Steel, 1980). Regression lines were fitted by the method of least squares. Significance was set at the 5 % level and means are presented as ±1 S.E.M.
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Results |
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Discussion |
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Despite these theoretical limitations, the maximum dive time recorded for freely diving star-nosed moles (47 s) exceeded the predicted maximum dive duration (32.3 s; 1.62M0.37) of Schreer and Kovacs (1997) by 45.5 %. In an earlier study of this species, Hickman (1984
) reported a maximum dive time of 19 s, but noted that one individual survived 2 min of forced submergence. By comparison, Calder (1969
) reported a maximum dive time of only 37.9 s in a single American water shrew (Sorex palustris) subjected to a forced dive. The average dive time of star-nosed moles (9.2 s) was comparable with that of the considerably larger mink (9.9 s, mass 850 g) (Dunstone and OConnor, 1979
) but shorter than the mean time recorded for freely diving juvenile muskrats (19 s, mass 254360 g) (MacArthur et al., 2001
). Few other empirical studies of diving behaviour exist for small-bodied, endothermic divers. Mean voluntary dive times are available for adult platypus (28 s, mass 9001500 g) (Evans et al., 1994
), European water shrews (36 s, mass 1020 g) (Ruthardt and Schröpfer, 1985
) and one 14 g American water shrew (5.7 s) (McIntyre, 2000
). It is noteworthy that the duration and frequency of voluntary dives by star-nosed moles were strongly influenced by water temperatures that are routinely encountered by this species in nature. MacArthur (1984a
) reported a similar finding for muskrats, and both studies suggest that thermoregulatory constraints affect dive performance in small-bodied endotherms.
The question remains, then, how does one account for the exceptional dive performance of the star-nosed mole? Potential factors contributing to the enhanced dive endurance of this species could include a strong dependence on anaerobic pathways during diving, a relatively low rate of oxygen depletion under water or higher-than-expected O2 reserves.
The absence of correlation between muscle buffering capacity and muscle Mb content suggests that variation in Mb content, and hence muscle aerobic capacity, is not matched by compensatory adjustments in the anaerobic potential of these muscles. Without adequate buffering capacity, even muscles possessing large glycogen deposits cannot function anaerobically for extended periods, because falling pH inhibits enzyme function and impedes further glycolytic activity (Castellini and Somero, 1981). The low buffering capacity of the skeletal muscles of star-nosed moles suggests little dependence on anaerobic metabolism while diving. This conclusion is supported by behavioural observations indicating that only 2.9 % of all voluntary dives exceeded the calculated ADL, a finding that may reflect the adoption of an aerobic diving schedule to maximize underwater search time and, hence, optimize foraging efficiency (Butler and Jones, 1997
).
Conventional estimates of DMR are often assumed to be approximately twice the BMR or RMR of the species in question (Burns and Castellini, 1996). Consistent with this assumption, the estimated DMR of star-nosed moles (5.38 ml O2 g1 h1) was 2.10xRMR (present study) and 2.39xBMR (2.25 ml O2 g1 h1) (Campbell et al., 1999
). However, these ratios are lower than that reported for muskrats (2.73xBMR) (MacArthur and Krause, 1989
). Moreover, the mean metabolic cost of surface swimming/diving of star-nosed moles was low compared with the mean value reported for mink (6.54 ml O2 g1 h1) (Stephenson et al., 1988
), suggesting that these insectivores display a relatively low mass-specific cost of submergence. Star-nosed moles, like muskrats, are strongly positively buoyant (mean specific gravity of moles 0.826±0.008, N=8) (McIntyre, 2000
), a factor that may contribute to the two- to threefold increase in the estimated cost of diving by these species. Marine birds that are almost neutrally buoyant, such as the Humboldt penguin Spheniscus humboldti, exhibit little change in
O2 during voluntary diving (Butler and Woakes, 1984
).
That body oxygen stores are often elevated in vertebrate divers appears well established (Butler and Jones, 1997; Kooyman and Ponganis, 1998
). Consistent with this trend, we found that the mean Hct of adult star-nosed moles (50.5 %) was similar to that of platypus (52 %) (Parer and Metcalfe, 1967
), but exceeded mean values reported for muskrat (39.146.8 %) (MacArthur et al., 2001
) and beaver Castor canadensis (42.1 %) (Kitts et al., 1958
). Combining lung, blood and muscle estimates, the mass-specific body O2 stores of adult star-nosed moles (34.0 ml kg1) (Table 3) exceed those estimated for platypus (25 ml O2 kg1) (Evans et al., 1994
), but fall within the range of values reported by MacArthur et al. (2001
) for summer- and winter-acclimatized muskrats (30.2 and 38.8 ml O2 kg1, respectively). A causal link between oxygen storage capacity and dive endurance is often assumed in interspecific comparisons (Kooyman, 1989
; Butler and Jones, 1997
), and our findings suggest that the exceptional diving ability of Condylura cristata may be attributed, at least in part, to elevated body O2 stores.
Comparisons of star-nosed moles with other fossorial mammals
A major objective of this study was to compare the O2 storage capacities of star-nosed moles and coast moles. The rationale for this comparison is the premise that several hypoxia-driven respiratory adaptations are potentially convergent in burrowers and divers, and it is informative to know the extent to which a reliance on diving has modified the O2 storage capacity of star-nosed moles. In making this comparison, we recognize that the phylogeny and evolutionary history of this family is not fully resolved and remains contentious. For instance, some workers have suggested that moles adopted fossorial habits following a period of aquatic adaptation (Campbell, 1939; Whidden, 1999
), while others have rejected this view, concluding instead that semi-fossorial and fossorial forms evolved directly from an ambulatory ancestor, without passing through a semi-aquatic phase (Reed, 1951
; Hickman, 1984
). However, it is important to stress that both Condylura cristata and the more recently derived Scapanus orarius passed through a specialized fossorial phase in their evolutionary development (Grand et al., 1998
), with the ancestral Condylura cristata either reverting towards or subsequently acquiring a semi-aquatic habit.
This controversy notwithstanding, our findings indicate that the mass-specific O2 stores of the star-nosed mole are 16.4 % greater than those of the coast mole (29.2 ml kg1). Interestingly, this difference is due mainly to interspecific variation in lung and muscle, rather than blood, O2 reserves (see below). The blood O2-carrying capacity of star-nosed moles (20.823.0 vol %) (Table 4) is relatively high, but comparable with those of other vertebrate divers including muskrat (20.624.1 vol %) (MacArthur et al., 2001) and platypus (23.0 vol %) (Grant, 1984
). Similarly, the blood O2-carrying capacity of coast moles (23.4 vol %) (Table 4), Townsends moles Scapanus townsendii (22.7 vol %) (Pedersen, 1963
) and the European mole Talpa europaea (23.3 vol %) (Quilliam et al., 1971
) is, as in other highly fossorial species including mole rats (20.2 vol %) (Ar et al., 1977
) and valley pocket gophers Thomomys bottae (22.8 vol %) (Lechner, 1976
), elevated relative to that of non-burrowing terrestrial mammals. These findings underscore the significance of this O2 storage compartment in vertebrates that routinely encounter hypoxia associated with diving or burrowing.
The skeletal muscle Mb concentration of the strictly fossorial coast mole (1.14 g 100 g1) was comparable with that of another burrowing mammal, the echidna (1.26 g 100 g1) (Hochachka et al., 1984), but substantially higher than for the semi-fossorial American shrew-mole (0.88 g 100 g1) (present study). This finding supports the argument that elevated muscle Mb concentrations are often associated with mammals highly specialized for a subterranean existence (Widmer et al., 1997
). However, muscle Mb concentration has also been shown to be a strong correlate of dive performance in mammalian divers (Kooyman and Ponganis, 1998
; Ponganis et al., 1999
). The relatively high Mb levels observed in Condylura cristata (1.36 g 100 g1) (Table 4) are consistent with values recorded for other semi-aquatic mammals, including platypus (1.43 g 100 g1) (Evans et al., 1994
), beaver (1.2 g 100 g1) (McKean and Carlton, 1977
) and seasonally acclimatized muskrats (1.211.38 g 100 g1) (MacArthur et al., 2001
). The tendency for the muscle Mb levels of star-nosed moles to exceed those of other subterranean mammals examined to date, including fossorial and semi-fossorial talpids, is noteworthy. It suggests that the adoption of a semi-aquatic lifestyle by this unique mole may have selected for enhanced muscle Mb levels, beyond those dictated by strictly fossorial habits.
Intraspecific variation in muscle myoglobin content
Skeletal muscle Mb concentration varied with age and sampling site in star-nosed moles. Confirming earlier studies, our results suggest that significant ontogenetic changes occur in muscle Mb levels. For instance, Ponganis et al. (1999) reported Mb levels for pre- and post-molt emperor penguin Aptenodytes forsteri chicks that were only 2431 % of adult values, whereas MacArthur et al. (2001
) found that the muscle Mb concentrations of juvenile muskrat cohorts varied closely with mass, ranging from 30.2 to 77.8 % of adult values. Noren et al. (2001
) recently reported age-dependant differences in muscle Mb concentration for a variety of diving marine endotherms, including the king penguin Aptenodytes patagonicus, the bottlenose dolphin Tursiops truncatus and the striped dolphin Stenella coeruleoalba, in which juvenile Mb values were 25, 57 and 68 % of adult values, respectively. Consistent with these trends, we found that the mean muscle Mb concentration of juvenile star-nosed moles was only 52.3 % of that measured in adults. Not surprisingly, the tendency for forelimb Mb levels to greatly exceed hindlimb values in Condylura cristata and Scapanus orarius is reversed from the trend generally observed in muskrats (MacArthur, 1990
; MacArthur et al., 2001
). Whereas the forelimb muscles of moles are the primary locomotor swimming and digging muscles, as reflected by their large relative mass, the hindlimbs of muskrats are the primary propulsive organs under water (Fish, 1982
).
Why a large lung volume in the star-nosed mole?
As noted above, differential partitioning of O2 stores was evident in the two talpid species examined. Of particular interest was our finding that the average lung volume of adult star-nosed moles (4.12 ml or 8.09 ml STPD 100 g1) was 1.81 times greater than the value predicted from allometry (2.28 ml) (Stahl, 1967). By comparison, the mean lung volume of coast moles (3.14 ml or 4.89 ml STPD 100 g1) conformed to standard allometric predictions. Lung O2 provides a large potential reserve in shallow-water divers (Snyder, 1983
) and contributed significantly to the total O2 storage capacity of star-nosed moles (Table 3). That this substantial reserve of O2 may be effectively exploited under water is supported by the observation that stripped Hbs of star-nosed moles from the same study population demonstrate exceptionally high oxygen-binding affinities (K. L. Campbell and R. E. Weber, unpublished data). The large lung volume of this species may also provide positive buoyancy during surface swimming, thus reducing the trunk surface area exposed to water and potentially minimizing the metabolic cost of aquatic thermoregulation. The sea otter Enhydra lutris also exhibits an exceptionally large lung volume that Costa and Kooyman (1984
) suggest facilitates floating at sea between periodic thermogenic bouts of activity.
Concluding remarks
The results of this study reveal that, like the coast mole, the star-nosed mole exhibits a large mass-specific blood O2 reserve. Whether this finding reflects convergence arising from diving- or burrowing-induced hypoxia, or instead is a trait conserved through lineage, is currently unknown. Star-nosed moles, however, possess more substantive lung and muscle Mb reserves, resulting in a greater total oxygen storage capacity, than for coast moles. We suggest that the additional need to attenuate heat loss associated with a semi-aquatic existence, perhaps combined with a need to augment O2 reserves for diving, may account for the exceptionally large lung volume and elevated Mb concentration observed in star-nosed moles. These traits, coupled with a high blood O2 storage capacity and a relatively low metabolic cost of underwater swimming, are probably key factors contributing to the impressive dive performance of this peculiar mammal.
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Acknowledgments |
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