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Water loss from aerially exposed mussels
J. exp. mar. Biol. Ecol., 1973, Vol. 12, pp. 145-155; @ North-Holland
WATER LOSS FROM AERIALLY
EXPOSED
Publishing Company
MUSSELS
N. COLEMAN ’ Zoology Department,
University
of Manchester,
England
Abstract: The valve activity and water loss from aerially exposed Mytilus edulis L. and Modiolus modiolus (L.) have been investigated in a series of laboratory experiments. Mytilus is capable of maintaining long periods of complete, or almost complete, valve closure when exposed in air, and this allows the retention of water in the mantle cavity and protects the tissues from evaporative water loss. Over periods of three days or more the amount of water lost from emersed Mytilus was found to be less than that retained in the mantle cavity at the beginning of exposure, suggesting that during normal periods of exposure the tissues are never directly subject to water loss. In contrast, Modiolus shows periods of gaping during which water loss is rapid due to drainage from the mantle cavity and evaporation from the tissues. The exposure of the tissues to air that results from gaping, makes the water loss susceptible to environmental influences of which wind was found to be the factor which caused the greatest increase in water loss and, as a consequence, an important factor in causing death through dehydration. The different abilities of Mytilus edulis and Modiolus modiolm to control water loss may be related to their intertidal distributions.
Desiccation during periods of aerial exposure is one of the greatest hazards facing intertidal animals, and it has been known for some time that the ability to control or withstand water loss is an important factor in controlling the zonation of littoral species, Gowanloch & Hayes (1926) showed that species of littorinids from high levels of the shore withstand desiccation better than do those from lower levels, and since then such a relationship has been shown in a number of other species (e.g., Brown, 1960). Kensler (1967) has further demonstrated that a similar pattern of zonation is found in littoral crevice fauna, the species that are least resistant to water loss living most deeply within a crevice. The mussels, Mytilus edulis L. and Modiolus modiolus (L.) both occur intertidally, the former more conspicuously so, and in comparing their responses to emersion an important difference in valve activity has been described (Coleman & Trueman, 1971). During aerial exposure Mytilus holds its valves closed, re-opening them only upon re-immersion. Under similar conditions Modiolus often shows periods of wide valve gape, during which opening may be in excess of that normally shown during immersion. The water losses of these two species have been studied in the laboratory in order to assess the importance of valve activity in controlling water loss during exposure. The findings are related to the intertidal distributions of the two species. 1 Present address: tralia.
Department
of Fisheries and Wildlife, 632 Bourke Street, Melbourne, 145
Aus-
146
N. COLEMAN MATERIALS ANI) METHOIN
Modiolus modiohs was obtained from the C!nivcrsity Marine Biological Station, Millport and the Marine Station, Port Et-in. Mytilus was collected from the shore at Conway, North Wales. The shelts of both species were scrubbed animals kept in a sea water aquarium at Manchester University. The mussels were exposed, in groups of ten or twelve. in desiccators
clean
and
the
whose internal
humidity was controlled by the use of saturated chemical solutions (Buxton & Mellanby, 1934; Solomon, 1951) or over sea water, and water loss was measured as decrease in weight. Weighing was carried out at the beginning and end of each period of exposure. During exposure at high humidities (when no control was needed) weighing was also carried out at intervals during the course of exposure. Before each weighing any moisture on the shell was wiped off with absorbant tissue. Each desiccator contained an Edney paper hygrometer, to measure humidity fluctuations caused by the introduction of the animals, a small fan, enabling the air to be circulated, and a small anemometer, to measure the velocity of the air current. Valve movements were either noted visually or were recorded with a movement transducer connected to a pen recorder (Narco Biosystems Inc.).
Measurement of the valve activity of MJifilus showed it to remain constant under all the conditions of exposure investigated. The response to exposure is that of complete, or almost complete, closure of the shell (Fig. 1) water being trapped in the mantle cavity so that the tissues are protected from the environment. Even when
Fig. 1. Effect of aerial exposure on the valve gape and heart rate of ~~r~~~~ u&&s: gape measured in
degrees and heart rate in beatsimin: period of exposure indicated by the horizontal line.
WATER
LOSS
FROM
MUSSELS
147
closure is not complete water loss is restricted because the edges of the mantle are held together across the persistent gape; however, as long as even a slight gape remains some water is lost. During the course of the experiments some individuals (about 4 % of the total) showed atypical behaviour, wide gaping leading to water losses in excess of normal. The initial response of Modiolus to aerial exposure is that of valve closure, but as the duration of exposure increases there is a tendency for the valves to open widely, often in excess of the normal filtering gape, so allowing water to drain from the 9
I:
0
I
,
4
HOURS
8
9-
6-
’ III
Fig. 2. Example
I I
of the effect of changing conditions of exposure on the valve activity of emersed activity of an individual exposed at 10 “C and R. H. 90 %; lower, same individual exposed at 20 “C and 90 % R. H.; gape measured in degrees; each vertical line represents one adduction, the top of the line being the gape at the beginning of adduction; no. of adductions during each hour indicated by the solid line, and the number of minutes in each hour during which the valves were completely closed by the broken line. Modiolus modiolus: upper,
N. COLEMAN
I48
mantle cavity and then to evaporate from the tissues. The valve movements of exposed and different individuals exposed to the same conditions may show great differences in the amount of time spent gaping, the width of gape, and the number of adductions. Nevertheless, the responses of the same individual to different conditions of exposure were generally found to be similar and changing the Modiolus are very variable
conditions
of temperature,
humidity,
and
wind
speed
did
not
bring
about
any
significant change in the valve movements shown by emersed Modioius. Ln Modiohs there is a relation between mussel size and the amount of water lost during exposure. Although the amount, by weight, of water lost is greater from large Modiolus than from small ones, the percentage loss (of the total weight) is less (Fig. 3): in Mytilus there was no relation between mussel size and water loss. A comparison of the percentage water losses from M.ytilus and Modiolus shows that the amount lost by Modiolus is significantly higher. except over very short periods, and becomes increasingly so as the duration of exposure increases. This is true when the Modiolus used are of the same size as the Myths to which they are compared (Fig. 4a) but because of the size-water loss relation in Modiolus large animals show a percentage loss similar to that of Mytilus (Fig. 4b), although the actual loss is much greater. In Modiolus water loss occurs in two phases, the first being the most rapid and corresponding to drainage of water from the mantle cavity. and the second slower and due primarily to evaporative loss from the tissues. The drainage of water from the
25
1
Fig. 3. The relationship between water loss and size, (shell length Modiolus modiolus: exposure for 26 h at 10 “C and 85-90 % R. H. l reduction in the total weight; U weight loss (g): regression lines for losses against size given. The regression coefficient for actual water and for percentage loss --3.34zk0.825.
in cm), for aerially exposed loss expressed as a percentage actual (A) and ‘A (P) water loss and size is 2.76110.6512
WATER LOSS FROM MUSSELS
149
mantle cavity occurs most noticeably during periods of wide gape but even when the shell is closed drainage may be fairly swift because of seepage through the byssal gap which is often well marked.
Fig. 4. The average water loss (“/oreduction of initial total weight) from groups of aerially exposed Myrilus edulis (My) and ~ud~#i~s ~~diol~~ (MO): a, individuals all with shell length 6.4-7.3 cm. b, Mytilusas (a) Mudiotus shell length 10.4-f 1.3cm. Exposure was at a constant temperature and in still air: vertical bars represent * 1 S.D.
To test that the rapid initial loss is due to loss from the mantle cavity estimates were made of the amount of water likely to be retained there at the beginning of exposure. Individuals of both species were taken from the aquarium, the shell dried, and the animal weighed. The posterior adductor muscle was then slit, the mussel opened out, water emptied from the mantle cavity, whose surfaces were lightly blotted, and the animal re-weighed. The change in weight was expressed as a percentage of the initial total weight. In both species the amount of water (“A total weight) retained in the mantle cavity is a function of size (Fig. 5). (The values may be slightly high since more water was removed than is the case if the mantle cavity is emptied simply by prizing the shell valves apart and allowing water to drain away, and slitting the adductor muscle may also have led to loss of body fluid.) In ~odio~~~ the amount of water estimated in this way agrees fairly closely with the amount of water lost in the first phase of aerial exposure (Fig. 6b). The time taken for all the water to drain from the mantle cavity was markedly different in the two species: in Modiolus all the water was lost within 6 h of exposure, whereas Myths commonly retained water for three days or more (Fig. 6a, b). The effects on Mytilus and Modiolus of exposure under different conditions of temperature and humidity, and in still and moving air are summarized in Table I. In all cases groups of 10-12 animals were used and exposure was for 6 h. The lower temperature used was that at which the animals had been kept, the upper temperature that
N. COLEMAN
I 50
b
Fig. 6. The relation between shell length (cm) and “/, total weight at the beginning of exposure due to the weight of the water retained in the mantle cavity: a) ~~di~~usF~u~~u~u$; b) ~ytilf4s cdulis: regression iines shown: the vertical bars ~1:I S.D. The regression coefficient for percentage mantle cavity water and size is -- 2.38_&0.7143 in M~d~ol~~s and -- 2.65&0,5919 in Mytilus.
54 36 T2 HOURS Fig. 6. The water loss from: a, three exposed Mytil~s r&&s, and b, two exposed ~~vdi~~~~ ~~di~fus: animais exposed in still air at a constant temperature and relative humid~ty~ arrows indicate point at which water lost is equal to the amount calculated from the regression lines in Fig. 5 asretainedin the mantle cavity at the beginning of exposure. I&
WATER LOSS FROM MUSSELS
151
TABLEI Water loss from groups of l&l2 Myths edulis and Modiolus modiolus exposed for periods of 6 h to different conditions of temperature, humidity and air movement. Species
Average weight* 1 S.D.
Conditions
of exposure
(8)
Myths Modiolus
Mytilus Modiolus Myths Modiolus Myths Modiolus Myths
edulis modiolus
edulis modiolus edulis modiolus edulis modiolus edulis
2.49*0.57 3.50*0.30
1.14hO.29 1.20*0.34 1.16f0.28 1.19f0.33 1.13&0.30 1.23f0.36 8.13+0.31
Modiolus
modiolus
5.88*1.34
Modiolus
modiolus
5.64&0.65
Myths Modiolus
edulis modiolus
20.29*4.3 6.66k1.32
Average water loss as % of total weight (incl. of shell and mantle cavity water)
Initial humidity Final humidity Temperature Still air
95 % 95 % 12 “C
Initial humidity Final humidity Temperature Still air
0% 45 % 12 “C
Initial R.H. Final R.H. Temperature Still air
0% 45 % 21 “C
Initial R.H. Final R.H. Temperature Moving air
0% 45 % 21 “C 758 ft/min
Initial R.H. Final R.H. Temperature Still air
10% 90 % 12 “C
Initial R.H. Final R.H. Temperature Still air
10% 90 % 25.3 “C
18.89
Initial R.H. Final R.H. Temperature Moving air
10% 50 % 25.3 “C 90 ft/min
4.5
6.44 17.28 4.5 12.23 4.49 15.93 3.65 27.95 8.86 13.95
38.70
such as might be encountered on a hot summer day. Changes in humidity caused by the introduction of the animals into the desiccators were noted and it was found that, especially with larger specimens, placing animals in the desiccators caused an immediate increase in humidity and the new humidity value did not noticeably change over a period of 6 h in still air, e.g., the introduction of Modiolus with an average weight of about 6 g into a desiccator with an internal humidity of 10 % caused the humidity to increase to, and remain at 90 %, Air movement in the desiccators was equivalent to a wind speed of Beaufort Force 4 or less and therefore within the limits commonly encountered on the shore. The water loss from Myths was found to be the same in all the conditions of exposure investigated, but that of Modiolus was found to be greatly affected by environmental factors, particularly that of wind. Alterations in humidity,
153
N. COLEMAN
and temperature increase alone had no significant effect on the water loss of Modiofus. At a low initial humidity and high temperature there was a tendency for increased water loss, but the mean values were not significantly higher than for conditions of low temperature and high humidity. The most profound influence on water loss from exposed Modiolus was found to be that of moving air. Even low windspeeds were found to cause an increase of almost 100 %, the extra water lost being due to increased evaporation from the tissues. In Modiolus it is difficult to establish with any certainty the percentage water loss resulting in death, since those animals used in the exposure experiments were only weighed at intervals and any found to be dead may have been so for some time and, since water loss continues even after death, may have lost more water than is fatal. Another source of error is the variation in the proportion of weight due to water retained in the mantle cavity, and a further difficulty arises from the fact that some Modioh although alive at the end of a period of exposure were dead within a day or two of re-immersion. An estimate of the water loss gave 40-50 O{)of the total weight (ix., weight inclusive of shell and mantle cavity water) for mortality. In the foregoing experiments water loss has been expressed as the percentage decrease in the total weight. Because this gives no indication of the loss suffered by the tissues, Modiolus were exposed after first having had the mantle cavity drained and, following exposure, the water loss is expressed as a percentage of the wet body weight. Establishment of the loss from the tissues which causes death is difficult for the reasons given above and also because of the difficulty of ensuring that before exposure
Fig. 7. Water modiolus: group
loss expressed as a “/, wet tissue wt from groups of three aerially exposed Modiolus a, exposed in moving air equivalent to a wind speed of Force 4; group b, exposed in still air: T and R.H. constant: vertical bars represent i-1 S.D.
WATER LOSS FROM MUSSELS
153
the mantle cavity is completely drained, but death was found to be the result of tissue losses of z 3040 % by weight. On one occasion a number of Modiolus showing gape almost as soon as they were exposed were separated into two groups and one exposed in still air and one in moving air. Exposure for 6 h in still air did not lead to lethal levels of water loss, but animals gaping in moving air died within 1 h of exposure; over a period of 6 h water losses of up to 80 % were recorded. DISCUSSION
The importance of the ability to remain shut during periods of aerial exposure becomes readily apparent when considering the water losses from Myths edulis and Modiolus modiolus. In Myths complete, or almost complete, valve closure effectively protects the tissues from the environment and reduces water loss to a minimum. During normal periods of exposure it is unlikely that the tissues are ever directly subject to water loss since the amount of water that is lost is usually much less than that retained in the mantle cavity at the beginning of exposure. Modiohs shows a marked contrast in its behaviour with a marked difference in water loss: the initial response to exposure is that of valve closure, but after a time, varying from a few minutes to two or three hours, the valves gape and water is allowed to drain from the mantle cavity and evaporate from the tissues. Exposure in still air for periods of two or three days may not lead to lethal levels of water loss but in wind death may occur rapidly, especially in individuals which begin to gape soon after the onset of exposure. Yet Kanwisher (1955) has shown that Modiolus can withstand the loss of as much as 65 % of its water content if this water is removed, at low temperatures, as ice. Despite its obvious importance as a factor affecting water loss the influence of wind on littoral molluscs has received surprisingly little attention although Kensler (1967) showed that, in comparison with exposure in still conditions, moving air causes a dramatic reduction in the survival time of the bivalve Lasaea rubra. The effect of wind on the behaviour and water loss of the gastropod Monodonta lineata has been described by Courtney (1972) who gives a water loss of 15-19 % of the wet body weight in two animals exposed for 2 h to a wind of 6 km/h, and of 6-27 % from animals exposed to a wind of 2 km/h for 6 h. These values are much lower than those found for Modiolus which, if gaping, may lose as much as 40 % after 1 h in a wind of 4 km/h. The large differences in loss between Monodonta and Modiohs may be explained in terms of the differences in structure between gastropods and bivalves. When Modiolus gapes the exposed body surface is large in comparison with the total body volume. In gastropods a proportionally smaller amount is exposed, even when the animal is crawling, and water loss may be even further reduced by the adherence of the animal to rock or other surfaces (Yonge, 1949; Brown, 1960) or by the closure of the shell with an operculum. The operculum has generally been considered to be of importance in reducing water loss but this may not inevitably be so as Gibson (1970) has shown for Thais.
154
N. COLEMAN
The differences in the intertidal distributions would be expected from their differing abilities
of Myths and Modiolus are such as to control water loss. Mytilus is pres-
ent on exposed surfaces, while Modiofus, except where it occurs sublittorally or in rock pools, is confined to positions on the shore where air movement will be sIight and humidity high, i.e., usually being found under large stones low on the shore, and often afforded further protection through being covered by fronds of seaweed. The distribution of tittoral animals is seldom governed by a single factor and a number of other causes need to be taken into account in considering the distribution differences of the two species. Gaping need not necessarily prove a bar to successful littoral colonization: Lent (1968, 1969) has shown that air gaping is one of the factors that has allowed Modiofus demfssus to become such a successful shore dweller. In this species the width of gape is more controlled than in M. ~odioIus and during exposure is equal to only about half the normat filtering gape, while water loss is further reduced by the infaunal position occupied during life. As with h4. demissus it is the ability to control valve activity in air that has allowed Myths edzalisto live successfully on the shore, but the consequences of retaining water in the mantle cavity appears to be more than just the avoidance of desiccation. Moon & Pritchard (1970) found that if M. cuf$mianus is clamped shut and exposed the oxygen content of the mantle cavity water falls to zero, whilst this water in normally exposed mussels remains 30-40 y{, saturated with oxygen. From this they inferred that 44. cali~r~~ia~l~.~ is capable of aerobic respiration during emersion. M. rdufis has been shown to be capable of respiring in air (Coleman, in press). In both cases the significance of aerial respiration is difficult to assess, for upon re-immersion both species show repayment of an oxygen debt, but the retention of mantle cavity water can be seen as providing the most suitable condition available for respiratory exchange. The tropical bivalve ~s~~~nu~o~afatus maintains a high heart rate during periods of aerial exposure and it has been suggested that in this species continued respiration may be facilitated by the ciliary circulation of water retained in the mantle cavity (Trueman & Lowe, 1971). Williams (1970) has attributed further importance to the retention of water in the mantle cavity. He suggests that the amount retained is sufficient to delay freezing of the tissues for some time after exposure to cold air and, because exposure is periodic, this could allow Mytihs to remain unfrozen from one period of immersion to the next. During the evolution of the Mytilidae the transition from an. infaunal (such as shown by ~odjofus de~issus and to a lesser extent M. ~rl~~fi~~f~s) to an epifaunal (such as shown by ~_y~iIu~) mode of life has been accompanied by structural changes as well as by changes in physiology and behaviour (1Stanley 1970, 1972). Of these physiological and behavioural changes an ability to control valve activity and maintain long periods of valve closure in response to aerial exposure has been of great importance in the colonization of exposed, intertidal surfaces.
WATER LOSS FROM MUSSELS
155
ACKNOWLEDGEMENTS
This work was carried out during the tenure of a grant from the Natural Environment Research Council. I am also grateful to Professor E. R. Trueman for his reading, and helpful criticism, of the original manuscript. REFERENCES BROWN, A. C., 1960. Desiccation as a factor influencing the vertical distribution of some South African gastropoda from intertidal rocky shores. Portugaliae Acta Biologica, B, Vol. 7, pp. 1 l-23. BUXTON,P. A. & K. MELLANBY,1934. The measurement and control of humidity. Bull. eat. Res., Vol. 25, pp. 171-176. COLEMAN,N., in press. The oxygen consumption of Mytitus edulis in air. Comp. Biochem. Physiol. COLEMAN,N. & E. R. TRUEMAN,1971. The effect of aerial exposure on the activity of the mussels Mytilus edulis L. and Modiolus modiolus (L.). J. exp. mar. Biol. Ecol., Vol. 7, pp. 295-304. COURTNEY,W. A. M., 1972. The effect of wind on shore gastropods. J. Zool. Lond., Vol. 166, pp. 133-139. GIBSON,J. S., 1970. The function of the operculum of Thais lupilha (L.) in resisting desiccation and predation. J. Anim. Ecol., Vol. 39, pp. 159-168. GOWANLOCH,J. N. & F. R. HAYES, 1926. Contributions to the study of marine gastropods. 1. The physical factors, behaviour, and intertidal life of Littorina. Contr. Can. Biol. Fish., Vol. 3, pp. 133-166. KANWISHER,J. W., 1955. Freezing in intertidal animals. Biol. Bull. mar. biol. Lab., Woods Hole, Vol. 109, pp. 56-64. KENSLER,C. B., 1967. Desiccation resistence of intertidal crevice species as a factor in their zonation. J. Anim. Ecol., Vol. 36, pp. 396-406. LENT, C. M., 1968. Air gaping by the ribbed mussel Modiolus demissus (Dillwyn): effects and adaptive significance. Biol. Bull. mar. biol. Lab., Woods Hole, Vol. 134, pp. 60-73. LENT, C. M., 1969. Adaptations of the ribbed mussel Modiolus demissus (Dillwyn) to the intertidal habitat. Am. Zool., Vol. 9, pp. 283-292. MOON, T. W. &A. W. PRITCHARD,1970. Metabolic adaptations in vertically separated populations of Mytilus californianus Conrad. J. exp. mar. Biol. Ecol., Vol. 5, pp. 35-46. SOLOMON,M. E., 1951. Control of humidity with potassium hydroxide, sulphuric acid or other solutions. BUN. ent. Res., Vol. 42, pp. 543-554. STANLEY,S. M., 1970. Relation of shell form to life habits in the Bivalvia (Mollusca). Mem. geol. Sot. Am., No. 125, 296 pp. STANLEY,S. M., 1972. Functional morphology and evolution of byssally attached bivalve molluscs. J. Paleont., Vol. 46, pp. 165-212. TRUEMAN,E. R. & G. A. LOWE, 1971. The effect of temperature and exposure on the heart rate of a bivalve mollusc, Isognomon al&us, in tropical conditions. Comp. Biochem. Physiol., Vol. 38A, pp. 555-564. WILLIAMS,R. J., 1970. Freezing tolerance in Mytitus edulis. Comp. Biochem. Physiol., Vol. 35, pp. 145-161. YONGE, C. M., 1949. The sea shore. Collins, London, 311 pp.
WATER LOSS FROM AERIALLY
EXPOSED
Publishing Company
MUSSELS
N. COLEMAN ’ Zoology Department,
University
of Manchester,
England
Abstract: The valve activity and water loss from aerially exposed Mytilus edulis L. and Modiolus modiolus (L.) have been investigated in a series of laboratory experiments. Mytilus is capable of maintaining long periods of complete, or almost complete, valve closure when exposed in air, and this allows the retention of water in the mantle cavity and protects the tissues from evaporative water loss. Over periods of three days or more the amount of water lost from emersed Mytilus was found to be less than that retained in the mantle cavity at the beginning of exposure, suggesting that during normal periods of exposure the tissues are never directly subject to water loss. In contrast, Modiolus shows periods of gaping during which water loss is rapid due to drainage from the mantle cavity and evaporation from the tissues. The exposure of the tissues to air that results from gaping, makes the water loss susceptible to environmental influences of which wind was found to be the factor which caused the greatest increase in water loss and, as a consequence, an important factor in causing death through dehydration. The different abilities of Mytilus edulis and Modiolus modiolm to control water loss may be related to their intertidal distributions.
Desiccation during periods of aerial exposure is one of the greatest hazards facing intertidal animals, and it has been known for some time that the ability to control or withstand water loss is an important factor in controlling the zonation of littoral species, Gowanloch & Hayes (1926) showed that species of littorinids from high levels of the shore withstand desiccation better than do those from lower levels, and since then such a relationship has been shown in a number of other species (e.g., Brown, 1960). Kensler (1967) has further demonstrated that a similar pattern of zonation is found in littoral crevice fauna, the species that are least resistant to water loss living most deeply within a crevice. The mussels, Mytilus edulis L. and Modiolus modiolus (L.) both occur intertidally, the former more conspicuously so, and in comparing their responses to emersion an important difference in valve activity has been described (Coleman & Trueman, 1971). During aerial exposure Mytilus holds its valves closed, re-opening them only upon re-immersion. Under similar conditions Modiolus often shows periods of wide valve gape, during which opening may be in excess of that normally shown during immersion. The water losses of these two species have been studied in the laboratory in order to assess the importance of valve activity in controlling water loss during exposure. The findings are related to the intertidal distributions of the two species. 1 Present address: tralia.
Department
of Fisheries and Wildlife, 632 Bourke Street, Melbourne, 145
Aus-
146
N. COLEMAN MATERIALS ANI) METHOIN
Modiolus modiohs was obtained from the C!nivcrsity Marine Biological Station, Millport and the Marine Station, Port Et-in. Mytilus was collected from the shore at Conway, North Wales. The shelts of both species were scrubbed animals kept in a sea water aquarium at Manchester University. The mussels were exposed, in groups of ten or twelve. in desiccators
clean
and
the
whose internal
humidity was controlled by the use of saturated chemical solutions (Buxton & Mellanby, 1934; Solomon, 1951) or over sea water, and water loss was measured as decrease in weight. Weighing was carried out at the beginning and end of each period of exposure. During exposure at high humidities (when no control was needed) weighing was also carried out at intervals during the course of exposure. Before each weighing any moisture on the shell was wiped off with absorbant tissue. Each desiccator contained an Edney paper hygrometer, to measure humidity fluctuations caused by the introduction of the animals, a small fan, enabling the air to be circulated, and a small anemometer, to measure the velocity of the air current. Valve movements were either noted visually or were recorded with a movement transducer connected to a pen recorder (Narco Biosystems Inc.).
Measurement of the valve activity of MJifilus showed it to remain constant under all the conditions of exposure investigated. The response to exposure is that of complete, or almost complete, closure of the shell (Fig. 1) water being trapped in the mantle cavity so that the tissues are protected from the environment. Even when
Fig. 1. Effect of aerial exposure on the valve gape and heart rate of ~~r~~~~ u&&s: gape measured in
degrees and heart rate in beatsimin: period of exposure indicated by the horizontal line.
WATER
LOSS
FROM
MUSSELS
147
closure is not complete water loss is restricted because the edges of the mantle are held together across the persistent gape; however, as long as even a slight gape remains some water is lost. During the course of the experiments some individuals (about 4 % of the total) showed atypical behaviour, wide gaping leading to water losses in excess of normal. The initial response of Modiolus to aerial exposure is that of valve closure, but as the duration of exposure increases there is a tendency for the valves to open widely, often in excess of the normal filtering gape, so allowing water to drain from the 9
I:
0
I
,
4
HOURS
8
9-
6-
’ III
Fig. 2. Example
I I
of the effect of changing conditions of exposure on the valve activity of emersed activity of an individual exposed at 10 “C and R. H. 90 %; lower, same individual exposed at 20 “C and 90 % R. H.; gape measured in degrees; each vertical line represents one adduction, the top of the line being the gape at the beginning of adduction; no. of adductions during each hour indicated by the solid line, and the number of minutes in each hour during which the valves were completely closed by the broken line. Modiolus modiolus: upper,
N. COLEMAN
I48
mantle cavity and then to evaporate from the tissues. The valve movements of exposed and different individuals exposed to the same conditions may show great differences in the amount of time spent gaping, the width of gape, and the number of adductions. Nevertheless, the responses of the same individual to different conditions of exposure were generally found to be similar and changing the Modiolus are very variable
conditions
of temperature,
humidity,
and
wind
speed
did
not
bring
about
any
significant change in the valve movements shown by emersed Modioius. Ln Modiohs there is a relation between mussel size and the amount of water lost during exposure. Although the amount, by weight, of water lost is greater from large Modiolus than from small ones, the percentage loss (of the total weight) is less (Fig. 3): in Mytilus there was no relation between mussel size and water loss. A comparison of the percentage water losses from M.ytilus and Modiolus shows that the amount lost by Modiolus is significantly higher. except over very short periods, and becomes increasingly so as the duration of exposure increases. This is true when the Modiolus used are of the same size as the Myths to which they are compared (Fig. 4a) but because of the size-water loss relation in Modiolus large animals show a percentage loss similar to that of Mytilus (Fig. 4b), although the actual loss is much greater. In Modiolus water loss occurs in two phases, the first being the most rapid and corresponding to drainage of water from the mantle cavity. and the second slower and due primarily to evaporative loss from the tissues. The drainage of water from the
25
1
Fig. 3. The relationship between water loss and size, (shell length Modiolus modiolus: exposure for 26 h at 10 “C and 85-90 % R. H. l reduction in the total weight; U weight loss (g): regression lines for losses against size given. The regression coefficient for actual water and for percentage loss --3.34zk0.825.
in cm), for aerially exposed loss expressed as a percentage actual (A) and ‘A (P) water loss and size is 2.76110.6512
WATER LOSS FROM MUSSELS
149
mantle cavity occurs most noticeably during periods of wide gape but even when the shell is closed drainage may be fairly swift because of seepage through the byssal gap which is often well marked.
Fig. 4. The average water loss (“/oreduction of initial total weight) from groups of aerially exposed Myrilus edulis (My) and ~ud~#i~s ~~diol~~ (MO): a, individuals all with shell length 6.4-7.3 cm. b, Mytilusas (a) Mudiotus shell length 10.4-f 1.3cm. Exposure was at a constant temperature and in still air: vertical bars represent * 1 S.D.
To test that the rapid initial loss is due to loss from the mantle cavity estimates were made of the amount of water likely to be retained there at the beginning of exposure. Individuals of both species were taken from the aquarium, the shell dried, and the animal weighed. The posterior adductor muscle was then slit, the mussel opened out, water emptied from the mantle cavity, whose surfaces were lightly blotted, and the animal re-weighed. The change in weight was expressed as a percentage of the initial total weight. In both species the amount of water (“A total weight) retained in the mantle cavity is a function of size (Fig. 5). (The values may be slightly high since more water was removed than is the case if the mantle cavity is emptied simply by prizing the shell valves apart and allowing water to drain away, and slitting the adductor muscle may also have led to loss of body fluid.) In ~odio~~~ the amount of water estimated in this way agrees fairly closely with the amount of water lost in the first phase of aerial exposure (Fig. 6b). The time taken for all the water to drain from the mantle cavity was markedly different in the two species: in Modiolus all the water was lost within 6 h of exposure, whereas Myths commonly retained water for three days or more (Fig. 6a, b). The effects on Mytilus and Modiolus of exposure under different conditions of temperature and humidity, and in still and moving air are summarized in Table I. In all cases groups of 10-12 animals were used and exposure was for 6 h. The lower temperature used was that at which the animals had been kept, the upper temperature that
N. COLEMAN
I 50
b
Fig. 6. The relation between shell length (cm) and “/, total weight at the beginning of exposure due to the weight of the water retained in the mantle cavity: a) ~~di~~usF~u~~u~u$; b) ~ytilf4s cdulis: regression iines shown: the vertical bars ~1:I S.D. The regression coefficient for percentage mantle cavity water and size is -- 2.38_&0.7143 in M~d~ol~~s and -- 2.65&0,5919 in Mytilus.
54 36 T2 HOURS Fig. 6. The water loss from: a, three exposed Mytil~s r&&s, and b, two exposed ~~vdi~~~~ ~~di~fus: animais exposed in still air at a constant temperature and relative humid~ty~ arrows indicate point at which water lost is equal to the amount calculated from the regression lines in Fig. 5 asretainedin the mantle cavity at the beginning of exposure. I&
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TABLEI Water loss from groups of l&l2 Myths edulis and Modiolus modiolus exposed for periods of 6 h to different conditions of temperature, humidity and air movement. Species
Average weight* 1 S.D.
Conditions
of exposure
(8)
Myths Modiolus
Mytilus Modiolus Myths Modiolus Myths Modiolus Myths
edulis modiolus
edulis modiolus edulis modiolus edulis modiolus edulis
2.49*0.57 3.50*0.30
1.14hO.29 1.20*0.34 1.16f0.28 1.19f0.33 1.13&0.30 1.23f0.36 8.13+0.31
Modiolus
modiolus
5.88*1.34
Modiolus
modiolus
5.64&0.65
Myths Modiolus
edulis modiolus
20.29*4.3 6.66k1.32
Average water loss as % of total weight (incl. of shell and mantle cavity water)
Initial humidity Final humidity Temperature Still air
95 % 95 % 12 “C
Initial humidity Final humidity Temperature Still air
0% 45 % 12 “C
Initial R.H. Final R.H. Temperature Still air
0% 45 % 21 “C
Initial R.H. Final R.H. Temperature Moving air
0% 45 % 21 “C 758 ft/min
Initial R.H. Final R.H. Temperature Still air
10% 90 % 12 “C
Initial R.H. Final R.H. Temperature Still air
10% 90 % 25.3 “C
18.89
Initial R.H. Final R.H. Temperature Moving air
10% 50 % 25.3 “C 90 ft/min
4.5
6.44 17.28 4.5 12.23 4.49 15.93 3.65 27.95 8.86 13.95
38.70
such as might be encountered on a hot summer day. Changes in humidity caused by the introduction of the animals into the desiccators were noted and it was found that, especially with larger specimens, placing animals in the desiccators caused an immediate increase in humidity and the new humidity value did not noticeably change over a period of 6 h in still air, e.g., the introduction of Modiolus with an average weight of about 6 g into a desiccator with an internal humidity of 10 % caused the humidity to increase to, and remain at 90 %, Air movement in the desiccators was equivalent to a wind speed of Beaufort Force 4 or less and therefore within the limits commonly encountered on the shore. The water loss from Myths was found to be the same in all the conditions of exposure investigated, but that of Modiolus was found to be greatly affected by environmental factors, particularly that of wind. Alterations in humidity,
153
N. COLEMAN
and temperature increase alone had no significant effect on the water loss of Modiofus. At a low initial humidity and high temperature there was a tendency for increased water loss, but the mean values were not significantly higher than for conditions of low temperature and high humidity. The most profound influence on water loss from exposed Modiolus was found to be that of moving air. Even low windspeeds were found to cause an increase of almost 100 %, the extra water lost being due to increased evaporation from the tissues. In Modiolus it is difficult to establish with any certainty the percentage water loss resulting in death, since those animals used in the exposure experiments were only weighed at intervals and any found to be dead may have been so for some time and, since water loss continues even after death, may have lost more water than is fatal. Another source of error is the variation in the proportion of weight due to water retained in the mantle cavity, and a further difficulty arises from the fact that some Modioh although alive at the end of a period of exposure were dead within a day or two of re-immersion. An estimate of the water loss gave 40-50 O{)of the total weight (ix., weight inclusive of shell and mantle cavity water) for mortality. In the foregoing experiments water loss has been expressed as the percentage decrease in the total weight. Because this gives no indication of the loss suffered by the tissues, Modiolus were exposed after first having had the mantle cavity drained and, following exposure, the water loss is expressed as a percentage of the wet body weight. Establishment of the loss from the tissues which causes death is difficult for the reasons given above and also because of the difficulty of ensuring that before exposure
Fig. 7. Water modiolus: group
loss expressed as a “/, wet tissue wt from groups of three aerially exposed Modiolus a, exposed in moving air equivalent to a wind speed of Force 4; group b, exposed in still air: T and R.H. constant: vertical bars represent i-1 S.D.
WATER LOSS FROM MUSSELS
153
the mantle cavity is completely drained, but death was found to be the result of tissue losses of z 3040 % by weight. On one occasion a number of Modiolus showing gape almost as soon as they were exposed were separated into two groups and one exposed in still air and one in moving air. Exposure for 6 h in still air did not lead to lethal levels of water loss, but animals gaping in moving air died within 1 h of exposure; over a period of 6 h water losses of up to 80 % were recorded. DISCUSSION
The importance of the ability to remain shut during periods of aerial exposure becomes readily apparent when considering the water losses from Myths edulis and Modiolus modiolus. In Myths complete, or almost complete, valve closure effectively protects the tissues from the environment and reduces water loss to a minimum. During normal periods of exposure it is unlikely that the tissues are ever directly subject to water loss since the amount of water that is lost is usually much less than that retained in the mantle cavity at the beginning of exposure. Modiohs shows a marked contrast in its behaviour with a marked difference in water loss: the initial response to exposure is that of valve closure, but after a time, varying from a few minutes to two or three hours, the valves gape and water is allowed to drain from the mantle cavity and evaporate from the tissues. Exposure in still air for periods of two or three days may not lead to lethal levels of water loss but in wind death may occur rapidly, especially in individuals which begin to gape soon after the onset of exposure. Yet Kanwisher (1955) has shown that Modiolus can withstand the loss of as much as 65 % of its water content if this water is removed, at low temperatures, as ice. Despite its obvious importance as a factor affecting water loss the influence of wind on littoral molluscs has received surprisingly little attention although Kensler (1967) showed that, in comparison with exposure in still conditions, moving air causes a dramatic reduction in the survival time of the bivalve Lasaea rubra. The effect of wind on the behaviour and water loss of the gastropod Monodonta lineata has been described by Courtney (1972) who gives a water loss of 15-19 % of the wet body weight in two animals exposed for 2 h to a wind of 6 km/h, and of 6-27 % from animals exposed to a wind of 2 km/h for 6 h. These values are much lower than those found for Modiolus which, if gaping, may lose as much as 40 % after 1 h in a wind of 4 km/h. The large differences in loss between Monodonta and Modiohs may be explained in terms of the differences in structure between gastropods and bivalves. When Modiolus gapes the exposed body surface is large in comparison with the total body volume. In gastropods a proportionally smaller amount is exposed, even when the animal is crawling, and water loss may be even further reduced by the adherence of the animal to rock or other surfaces (Yonge, 1949; Brown, 1960) or by the closure of the shell with an operculum. The operculum has generally been considered to be of importance in reducing water loss but this may not inevitably be so as Gibson (1970) has shown for Thais.
154
N. COLEMAN
The differences in the intertidal distributions would be expected from their differing abilities
of Myths and Modiolus are such as to control water loss. Mytilus is pres-
ent on exposed surfaces, while Modiofus, except where it occurs sublittorally or in rock pools, is confined to positions on the shore where air movement will be sIight and humidity high, i.e., usually being found under large stones low on the shore, and often afforded further protection through being covered by fronds of seaweed. The distribution of tittoral animals is seldom governed by a single factor and a number of other causes need to be taken into account in considering the distribution differences of the two species. Gaping need not necessarily prove a bar to successful littoral colonization: Lent (1968, 1969) has shown that air gaping is one of the factors that has allowed Modiofus demfssus to become such a successful shore dweller. In this species the width of gape is more controlled than in M. ~odioIus and during exposure is equal to only about half the normat filtering gape, while water loss is further reduced by the infaunal position occupied during life. As with h4. demissus it is the ability to control valve activity in air that has allowed Myths edzalisto live successfully on the shore, but the consequences of retaining water in the mantle cavity appears to be more than just the avoidance of desiccation. Moon & Pritchard (1970) found that if M. cuf$mianus is clamped shut and exposed the oxygen content of the mantle cavity water falls to zero, whilst this water in normally exposed mussels remains 30-40 y{, saturated with oxygen. From this they inferred that 44. cali~r~~ia~l~.~ is capable of aerobic respiration during emersion. M. rdufis has been shown to be capable of respiring in air (Coleman, in press). In both cases the significance of aerial respiration is difficult to assess, for upon re-immersion both species show repayment of an oxygen debt, but the retention of mantle cavity water can be seen as providing the most suitable condition available for respiratory exchange. The tropical bivalve ~s~~~nu~o~afatus maintains a high heart rate during periods of aerial exposure and it has been suggested that in this species continued respiration may be facilitated by the ciliary circulation of water retained in the mantle cavity (Trueman & Lowe, 1971). Williams (1970) has attributed further importance to the retention of water in the mantle cavity. He suggests that the amount retained is sufficient to delay freezing of the tissues for some time after exposure to cold air and, because exposure is periodic, this could allow Mytihs to remain unfrozen from one period of immersion to the next. During the evolution of the Mytilidae the transition from an. infaunal (such as shown by ~odjofus de~issus and to a lesser extent M. ~rl~~fi~~f~s) to an epifaunal (such as shown by ~_y~iIu~) mode of life has been accompanied by structural changes as well as by changes in physiology and behaviour (1Stanley 1970, 1972). Of these physiological and behavioural changes an ability to control valve activity and maintain long periods of valve closure in response to aerial exposure has been of great importance in the colonization of exposed, intertidal surfaces.
WATER LOSS FROM MUSSELS
155
ACKNOWLEDGEMENTS
This work was carried out during the tenure of a grant from the Natural Environment Research Council. I am also grateful to Professor E. R. Trueman for his reading, and helpful criticism, of the original manuscript. REFERENCES BROWN, A. C., 1960. Desiccation as a factor influencing the vertical distribution of some South African gastropoda from intertidal rocky shores. Portugaliae Acta Biologica, B, Vol. 7, pp. 1 l-23. BUXTON,P. A. & K. MELLANBY,1934. The measurement and control of humidity. Bull. eat. Res., Vol. 25, pp. 171-176. COLEMAN,N., in press. The oxygen consumption of Mytitus edulis in air. Comp. Biochem. Physiol. COLEMAN,N. & E. R. TRUEMAN,1971. The effect of aerial exposure on the activity of the mussels Mytilus edulis L. and Modiolus modiolus (L.). J. exp. mar. Biol. Ecol., Vol. 7, pp. 295-304. COURTNEY,W. A. M., 1972. The effect of wind on shore gastropods. J. Zool. Lond., Vol. 166, pp. 133-139. GIBSON,J. S., 1970. The function of the operculum of Thais lupilha (L.) in resisting desiccation and predation. J. Anim. Ecol., Vol. 39, pp. 159-168. GOWANLOCH,J. N. & F. R. HAYES, 1926. Contributions to the study of marine gastropods. 1. The physical factors, behaviour, and intertidal life of Littorina. Contr. Can. Biol. Fish., Vol. 3, pp. 133-166. KANWISHER,J. W., 1955. Freezing in intertidal animals. Biol. Bull. mar. biol. Lab., Woods Hole, Vol. 109, pp. 56-64. KENSLER,C. B., 1967. Desiccation resistence of intertidal crevice species as a factor in their zonation. J. Anim. Ecol., Vol. 36, pp. 396-406. LENT, C. M., 1968. Air gaping by the ribbed mussel Modiolus demissus (Dillwyn): effects and adaptive significance. Biol. Bull. mar. biol. Lab., Woods Hole, Vol. 134, pp. 60-73. LENT, C. M., 1969. Adaptations of the ribbed mussel Modiolus demissus (Dillwyn) to the intertidal habitat. Am. Zool., Vol. 9, pp. 283-292. MOON, T. W. &A. W. PRITCHARD,1970. Metabolic adaptations in vertically separated populations of Mytilus californianus Conrad. J. exp. mar. Biol. Ecol., Vol. 5, pp. 35-46. SOLOMON,M. E., 1951. Control of humidity with potassium hydroxide, sulphuric acid or other solutions. BUN. ent. Res., Vol. 42, pp. 543-554. STANLEY,S. M., 1970. Relation of shell form to life habits in the Bivalvia (Mollusca). Mem. geol. Sot. Am., No. 125, 296 pp. STANLEY,S. M., 1972. Functional morphology and evolution of byssally attached bivalve molluscs. J. Paleont., Vol. 46, pp. 165-212. TRUEMAN,E. R. & G. A. LOWE, 1971. The effect of temperature and exposure on the heart rate of a bivalve mollusc, Isognomon al&us, in tropical conditions. Comp. Biochem. Physiol., Vol. 38A, pp. 555-564. WILLIAMS,R. J., 1970. Freezing tolerance in Mytitus edulis. Comp. Biochem. Physiol., Vol. 35, pp. 145-161. YONGE, C. M., 1949. The sea shore. Collins, London, 311 pp.