1. The mechanical power required by Nymphon for swimming at constant depth has been calculated from drag forces acting on the legs. For an adult male this was found to be 3·4 W kg. Only about 60 % of this is used to support the animal’s weight in water.

  2. The metabolic rate fluctuates spontaneously over a tidal cycle, being greatest during the ebb-tide period. The mean rate of oxygen consumption during the animals least active phase was found to be about 0·1 µl O2 mg−1 h−1.

  3. The total carbohydrate and lipid immediately available for combustion have been estimated at 4·64 and 16 µg/mg wet wt respectively. These quantities should be adequate for about 42 h periodic swimming in an adult Nymphon.

Although normally a benthic animal, Nymphongracile undergoes frequent swimming excursions, especially when denied access to a suitable substrate in the laboratory. This periodic swimming is endogenously controlled, with a rhythm which persists for at least 56 h under constant conditions (Isaac & Jarvis, 1973). In the sea, swimming may be induced by the cyclical pressure changes associated with the tide (Morgan, Knight-Jones & Nelson-Smith, 1964) and the field observations of Fage (1932) suggest that at certain times of the year Nymphon may spend quite long periods in the plankton.

Many of the more permanent members of the plankton have skeletal spines or bristles which help to slow down their rate of descent through the water (e.g. see Friedrich, 1969).

Nymphon, however, has a density greater than that of sea water, and despite having a large surface area relative to its volume the animal can only swim upwards or hold station at constant depth by beating its legs continuously. The relationship between the power required for swimming and the animals’ energy reserves will thus be significant in determining the duration of the pelagic phase, and the energy budget of Nymphon gracile while swimming at constant depth is investigated here.

Animals were collected at low water from the shore at Mumbles Point, South Wales, during the months of October and November and transported immediately to a constant-environment room in the Zoology Department at the University of Birmingham. Although almost fully grown, the animals are not sexually mature at this time (King & Jarvis, 1970) so measurements of metabolic rate and fuel reserves were unaffected by reproductive activity.

Swimming activity was recorded on ciné film as described previously (Morgan, 1971) and by direct observation at intervals of 30 min. The different levels of activity were scored on a 0−5 scale (cf. Morgan, Knight-Jones & Nelson-Smith, 1964), animals standing motionless on the bottom scoring o, and those swimming clear scoring 5.

Oxygen uptake was measured using a modified Winkler technique. The respiratory chambers were 40 ml Perspex bottles fitted with a rubber bung and a short length of rubber tubing sealed by a screw clip. Samples of sea water of 20 ml were removed by means of a hypodermic needle and syringe, and manganous and manganic hydroxide were precipitated in the barrel of the syringe by the addition of manganous chloride, sodium hydroxide and potassium iodide solutions. The precipitate was dissolved by the further addition of concentrated hydrochloric acid, and the solution transferred to small conical flasks where the liberated iodine was titrated against sodium thiosulphate in the conventional manner. Three respiratory chambers, each containing between 7 and 25 Nymphon, together with a control vessel of sea water alone, were placed in a water bath equilibrated to room temperature in a constant temperature room at 12 °C. Measurements of dissolved oxygen were taken at approximately 2 h intervals and the sea water in the respiratory and control vessels changed after each sampling.

Specimens to be used in the biochemical analyses were weighed before being frozen in sea water and kept at − 25 °C until they were used, usually about 24 h later. An estimate of the animals’ fuel reserves was obtained from an analysis of the carbohydrates, lipids and amino acids present in whole animal homogenates. Lipids were extracted from aqueous homogenates in a mixture of chloroform and methanol, and analysed by thin-layer and gas-liquid chromatography. The carbohydrate content of a further portion of the same homogenate was assayed as neutral monosaccharides after reduction with concentrated sulphuric acid, using the method of Hough, Jones and Wusteman (1971). The concentration of free body sugars was similarly investigated using unhydrolysed extracts. Free amino acids were extracted in 70% ethanol and then subjected to standard analysis in a Locarte automatic analyser. Total body protein was estimated as amino acids extracted from a further homogenate, in 50 % pyridine to separate the tissue protein from the cuticle.

The instantaneous energy required to move each segment of the leg at different stages during the cycle of movement was derived from previously calculated force values (Morgan & Hayes, 1977) and from the velocity in the line of action of the force. Drag forces acting both normal and tangential to the segment were considered and the power produced by the entire leg during a single beat of low elevation was thus calculated. From this an estimate of the energy expended by Nymphon when swimming at constant depth was obtained.

Oxygen uptake

When kept under constant conditions in the laboratory Nymphon shows an endogenous rhythm of tidal frequency. In freshly collected animals maximum swimming activity occurs about 1 h after the time of expected high water, but the peaks drift progressively later by about 2−3 h in each successive cycle (Isaac & Jarvis, 1973). These observations are confirmed here. Fig. 1,a shows that the spontaneous swimming activity of five animals, each kept in a separate 250 ml flask under constant conditions in the laboratory, is maximal during the ebb-tide period. Oxygen uptake of another group of animals measured over a similar period (see Methods) is shown in Fig. 1 (6). A clearly defined peak in the rate of oxygen uptake occurred about 3 h after the time of the second high water following collection. Earlier during the ebb, and during the flood-tide period, the rate of oxygen uptake was much lower, with a mean value of approximately 0·1 µl O2 mg−1 h−1.

The animals in the respiratory chambers were not seen to swim at any time during the experiment, but remained in a cluster with their legs entangled together. Nevertheless the animals appeared to be more excited, and individuals grappled together within the groups with greater vigour, during the ebb-tide period.

Fuel resources

The lipid content of three samples, containing between 29 and 157 mg wet wt of pycnogonid was analysed as indicated earlier (see Methods) and the results are shown in Table 1. Cholesterol, triglycerides and phospholipids occur in fairly constant proportions in each of the three groups, and between them account for about 60% of the total body lipid. Cholesterol alone accounts for less than 10% while the triglycerides and phospholipids each constitute about a further 25 % The proportion of unidentified lipid, on average about 40%, varies rather more between the groups, but not significantly so. Not all the total body lipid is likely to be available for combustion. Phospholipids are probably bound up in the tissues, and assuming that Nymphon is unable to break down cholesterol, the total lipid energy reserve would be just under 16 µg per mg wet wt of pycnogonid.

The proportion of different monosaccharide sugars in the hydrolysed extract was also fairly constant between the three groups, as may be seen from Table 2. Glucose is clearly the most common sugar (50%), and together with mannose constitutes approximately 70% of the total monosaccharides present. The proportion of ribose varies between samples rather more than the other sugars, but on average accounts for between 11 and 12% of the total. The remaining sugar is made up mainly of galactose (6−7% of the total) and xylose and arabinose which occur in trace quantities only. Of the total carbohydrate present, the ribose sugars are likely to occur in the nucleus, ribosomes, or as transfer RNA, while other sugars will be bound up with amino acids as chitin. Analysis of unhydrolysed homogenates indicates that, on average, only about 26·7 % of the total carbohydrate occurs as free sugar, mainly in the form of polysaccharides, and on this basis the quantity of carbohydrate immediately available for combustion works out at only 4·64 µg per mg wet wt of pycnogonid.

Excluding the cuticular proteins, amino acids were found to account for less than 1% of the wet wt of Nymphon, there being 187 ·5 µg-1 wet wt. Most of this appears to be bound up in the tissue proteins, however, for analysis of an unhydrolysed homogenate indicated that free amino acids were present in only much smaller quantities, in total less than 0 ·9 µg mg−1 wet wt.

Calculated energy expenditure

The energy expended during the movement of individual leg segments was calculated as described in the Methods section, and summated over the entire leg. The instantaneous energy required at different stages in the beat of a single leg for an animal holding station at constant depth is shown in Fig. 2. From these values the integral energy per beat was found to be 111 × 10−7J, with a power output of 1 ·057 ×10−5 W (= 2 ·53 × 10−6 cal/s). Assuming the beat of each leg to be identical the total power output of all eight legs while swimming at constant depth would be 8 ·76 × 10−6 W or 0 ·073 cal h−1. The ovigerous male Nymphon for which these values were calculated weighed 37 mg, to which the egg masses contributed 12 mg, so the energy required for swimming works out at 3 ·5 W kg or 0 ·0029 cal mg−1 wet wt. pycnogonid h−1. Not all of this is used in supporting the body in the water, however, and a considerable proportion is used in moving the leg segments laterally through the water, as may be seen from Fig. 2. For the low elevation beat investigated this proportion was found to be 27 ·5 × 10−7 J, approximately 25% of the total energy output during the beat. The remaining 73 % of the energy is used in moving water vertically, and, calculating from the force values derived earlier (Morgan & Hayes, 1977) just over 8%, approximately 9 × 10−7 J per beat, would be used in producing a downward force during the recovery stroke. This would have to be offset against the remaining energy component, so that the energy used in supporting the animals weight in water would be 75% − (2 × 8%) = 59%.

As the legs beat in a vertical plane much of the energy produced during the power stroke is kinetic energy which is regenerated during the recovery (Morgan & Hayes 1977). The mass of the legs has not been considered in the above calculations, and although the overall energy budget is unaffected, the useful energy during the power and recovery strokes (i.e. that providing upward lift) will be respectively less and greater than the proportions estimated above.

The rate of oxygen consumption of a resting Nymphon, 0 ·1 l O2 kg−1 h−1, is of the same order of magnitude as that of sedentary or sessile marine arthropods, for example the barnacles Balanus balanus and B. balanoides (Barnes, Barnes & Finlayson, 1963). Assuming 1 cm8 of oxygen to support metabolism releasing about 1 J whatever the food, this is equivalent to about 0 ·56 W kg−1. Active swimming results in an increase in metabolism, and the mechanical power required per unit mass is 3·5 W kg−1. Assuming a 25 % energy transformation at the muscle the chemical power required for swimming would be 14 W kg−1. This is considerably higher than the 1 W kg−1 predicted by the increase in rate of oxygen uptake measured over the endogenous activity rhythm. However, the animals in the respiratory chambers did not actually swim during the experiment. Some attempted to do so, but it is unlikely that all the animals present would have swum. Even when stimulated by falling pressure only about 60 % have been observed to be active at any one time in similar experiments (Morgan, Knight-Jones & Nelson-Smith, 1964), and the peak rate of oxygen uptake recorded above (Fig. 1) is probably much lower than would be expected for a swimming animal. The power requirement for swimming therefore has been taken to be about 14 W kg−1.

Prolonged swimming excursions normally occur only in arrhythmic laboratory animals (Isaac & Jarvis, 1973). Freshly collected animals swim intermittently, being clear of the bottom for only about 30 % of the time (Morgan, in preparation) and the mean power requirement is therefore 0 ·56 W + (0 ·3 + 14) W = 4 ·76 W kg−1. The available food resources are 16 g kg−1 of lipid and 4 ·6 kg−1 of carbohydrate which, with heats of combustion of about 40 and 17 MJ kg−1 respectively represent an energy store of 720000 J kg−1. Used at a rate of 4 ·76 W kg−1 this should last for just over 42 h. About 9 −10 h elapsed between collecting Nymphon and their refrigeration prior to biochemical analysis, and it seems reasonable to suppose that freshly collected animals would have adequate fuel for approximately 52 h rhythmic swimming. It is interesting to note therefore that the animals studied by Isaac & Jarvis (1973) became inactive after about 56 h and eventually died. It is likely that the continued survival of unfed animals after this period would depend on the mobilization of tissue carbohydrates and proteins, perhaps from the cuticle as Florey (1966) has suggested.

An estimation of the efficiency of the swimming stroke is complicated by the fact that when holding station the body does not move and the legs technically do not do any work. Moreover a comparison of drag on the legs during the power and recovery strokes is perhaps not as meaningful for Nymphon as for more conventional paddle swimmers (e.g. see Nachtigall, 1961a, b;Alexander, 1968). Not only do the terminal segments of the leg produce an upward propulsive force during the recovery, but tha elevation of the leg during this phase generates a kinetic energy which is released during the power stroke. If, however, we consider that, of the total energy expended during the movement of the leg, only that used in supporting the weight of the body, Ew, is usefully employed, then a measure of the total overall efficiency of the leg beat is given by Ew/(Ew+2Ed+ El, where E1 is the component of energy used in moving water laterally and Ea is the downward directed lift, produced mainly during the recovery stroke. For the low elevation beat investigated the efficiency factor thus calculated would be 0 ·59, which is considerably lower than a comparable factor calculated for the freshwater beetles Acilus and Gyrinus by Nachtigall (1961b).

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