Download THE ADAPTATION OF GUNDA ULVAE TO SALINITY

6.3
THE ADAPTATION OF GUNDA ULVAE
TO SALINITY
I. THE ENVIRONMENT
BY C. F. A. PANTIN, MA.
(From the Zoological Laboratory, Cambridge, and the
Marine Biological Laboratory, Plymouth.)
(Received ist October, 1930.)
(With One Text-figure.)
WHEREAS it
is well known that most organisms cannot survive sudden large changes
in the salinity of the external medium yet estuarine organisms have developed
powers of resistance to them. Recent work, particularly that of Schlieper (1929),
has thrown some light on the behaviour of estuarine animals in diluted sea water.
In most estuarine animals the salinity variations of the environment fall far
short of the change from completely fresh water to undiluted sea water. But the
triclad worm, Gunda ulvae, is found where variations of this magnitude may be
expected with each tide, for it inhabits the sea shore at the estuaries of very small
streams.
The ability of these worms to withstand these changes is the more remarkable
because of their small size, and because they are not covered with a protecting
cuticle which might render them impervious to environmental osmotic changes.
Moreover, whereas coelomates may mitigate the effect of such changes upon their
cells by control of the composition of their body fluids, Gunda possesses no body
cavity.
Salinity variations may be expected to influence greatly the water exchange
of Gunda, and experiments showed that this was true (Weil and Pantin, 1931;
Pan tin, 1931). But it was soon found that in order to interpret these experiments
an accurate description of the environment was required.
Little attention has yet been paid to the immediate physical and chemical
environment in which an estuarine organism lives. Thus, although Gunda lives
definitely in association with fresh water, it seems possible that by suitable changes
of position it might avoid gross changes in salinity. Reid (1930) found that in a
small stream flowing over a sandy shore water deep in the sand may retain a fairly
high salinity at low tide. It is therefore necessary to determine the exact distribution of the Gunda and the salinity variations in its neighbourhood.
64
C. F. A. PANTIN
Further, experiments on the salt exchange of these worms when exposed
fresh water showed that the chemical composition of this water was a factor of
prime importance. The mere description of salinity changes is inadequate: the
problem of estuarine existence is not one of simple dilution but of dilution accompanied by changing chemical composition, a factor which may vary in every river.
Indeed, when speaking of estuarine conditions, the term "fresh water" is far too
wide, .and may cover waters which differ among themselves almost as much as
any of them do from sea water. It was therefore necessary to determine the composition of the water flowing by the Gunda in their natural habitat.
THE MEDIUM.
Gunda ulvae is found in large numbers in the estuary of a small stream at
Wembury (South Devon) where this flows over an open foreshore. It is not found
except in association with both fresh water and sea water. The external medium
consists entirely of mixtures of stream water with Atlantic sea water.
The following methods were used to analyse the stream water. A large sample
of stream water was collected on July 23rd, 1930, and the following constituents
determined:
(1) Total solids, by evaporation to dryness on a water bath, followed by heating
to 1800 C. to constant weight.
(2) Carbonates, by titration while boiling with H2SO4 to/>H 7, using phenol red.
(3) Chlorides, by titration by Mohr's method with AgNO3 (Treadwell and Hall,
1928).
(4) Sulphates, determined as BaSO4 using the turbidimetric method of Thresh
and Beale (1925).
(5) Calcium, by conversion to oxalate and titration with KMnO4 (Treadwell
and Hall, 1928).
(6) Magnesium, determined as phosphate in the nitrates from (5) using the
turbidimetric method of Thresh and Beale (1925).
(7) Sodium andpotassium, by removal of SO4, Mg and Ca; conversion to chloride,
and the dry weight compared with the AgNO3 titre. The method estimates accurately
the total alkali metals present but does not give accurately the proportion of Na
to K. The exact determination of this was not considered necessary.
Four sets of independent determinations of each constituent were made. The
maximal and minimal values found'are shown in Table I.
The stream water is a typical hard water containing in addition to CaCO3
a large amount of Mg and SO4. The high alkali chlorides probably result from the
cultivation of the land through which it flows. In winter the Cl' rises and the
CO 3 " falls (column 4). The change in salt concentrations is, however, far smaller
than the change in volume of water in the stream.
The other component of the mixture in the estuary is Atlantic sea water, the
composition of which is shown in Table I. This was calculated from Dittmar's
(1884) analysis.
The Adaptation of Gunda ulvae to Salinity
Table I.
Milligrammes per litre.
Wembury stream water
Atlantic sea water
calculated from
Dittmar (1884)
July 23rd, 1930
co3
Cl
so
Ca4
Mg
Na
K
Sum
Total solids found
*H
Maximum
Minimum
1194
41-3
24-6
647
14-4
1188
918
408
50-0
24-3
—
632
3085
291-4
3*9
317
58-4
—
—
—
—
—
—
77
246
I9S
78
13-9
17-5
129
0073
19-64
2-69
0-42
131
10-70
0-39
35-22
x 10s
x io 3
xio*
x 10s
xio3
xio3
xio3
xio3
—
82
HABITAT.
Gunda is found under stones in the estuary of the Wembury stream. It is rarely
found beneath stones less than 15 cm. in diameter, probably because these are
subject to violent movement in rough weather.
The stream itself rises in the Staddon grits and flows over Middle and Lower
Devonian slates and grits. The basin is about 2 miles long and contains much
cultivated ground. The stream flows rapidly and varies considerably in volume
according to the season. In July 1930 it was roughly 1 to \\ m. in width and
10-15 c m - deep at the mouth. It may reach many times this volume in winter.
It debouches into a fresh-water pool (about 5 m. x 25 cm. deep) at the top of
a beach of shingle (Fig. 1) in Wembury Bay. Beyond the pool is a shelf of shingle
thrown up by the highest tides. The shingle consists of stones averaging 3-5 mm.
in diameter, together with larger stones and boulders. The stream cuts through this
" beach shelf" and flows rapidly down to the edge of the shingle (Station E, Fig. 1).
In the next section (Stations E-M) it flows through channels and pools in the
rocks with some fine shingle and large stones in its bed. Beyond Station M (Fig. 1)
the stream flows between rocks and sand.
The bed of the stream in the middle section of the estuary (Stations E-M) is
fairly constant. But the course through the shingle varies greatly in rough weather,
and much of the water in this region flows through the shingle and not on the
surface. Thus, from July 15th to 19th, 1930, the stream flowed from the pool
over the shingle, decreasing to about one-half of the volume on the land above the
pool; reappearing full-size round Station E. The sea was calm and the bed of the
stream fairly constant. From July 28th till August 1st the stream disappeared into
shingle at the end of the pool, reappearing as several small springs 10-20 m. down
the beach. The sea was then rough, and the shingle altered each tide.
JEB-VIIli
S
66
C. F. A. P A N T I N
Observations were made in the fresh-water pool, P, and at Stations A-]VH
extending down the estuary to a point beyond the occurrence of Gunda. The levels
and distances of the more important stations were surveyed for me by Mr M. A.
Spender. These are shown in the vertical section in Fig. i, together with the
heights of tides. T h e latter are based on the Devonport Chart Datum for tides in
the Hamoaze. The observed tides at Wembury agreed well with these except that,
when the sea was rough on July 28th, 1930, large breakers swept above the level of
high-water spring tides and entered the fresh-water pool.
Fresh-water pool
Lowest record ol freshwater fauna, July 1930: Level of beach sheU.
Desert region
Upper limit of Ounda and
Pntoiribu
Upper limit of Enteromorpha
• Lower limit of Gunda and
I
Pmtodrilu*
40
/•» /"» r\
-Shingle
/ / / / /
« Bock + boulders
50
60
80
90
100
1 10
Metres below pool
(measured along bed of stream)
Density of Gunda population along stream
Fig. i. Vertical section along estuary of stream, showing substratum and limits of organisms, etc.
At spring tides, July 28th, 1930, fresh-water fauna pushed back to pool, and upper limit of Gunda
at Station D.
The fauna showed a regular sequence from a very rich fresh-water fauna in the
pool to a normal marine shore fauna. The following collections made are typical.
FRESH-WATER POOL P.
Platyhelminth.es
Hirudinea
Gastropoda
Crustacea
Insecta
Polycelis cornuta1
Glossosiphonia heteroclita
Herpobdella atomaria
Rissoa ventrosa
Gammarus pulex
Larvae of Ephemerida; Plecoptera;
Chironomidae; Trichoptera
1
This organism agrees perfectly with the description (Whitehead, H., 1921), although it has
been suggested that it is restricted in habitat to high land in a manner similar to Planaria alpina
(Hubault, 1927).
The Adaptation of Gunda ulvae to Salinity
STATION B.
Nil.
STATIONS C AND D.
Platyhelminthes
Archiannelida
Gunda ulvae
Unidentified Acoelan
Protodrilus flavocapitatus
STATIONS E, F, G AND H.
Platyhelminthes
Archiannelida
Crustacea
Gunda ulvae
Protodrilus flavocapitatus
Gammarus sp. (undescribed)
Jaera marina
STATION K.
Coelenterata
Platyhelminthes
Archiannelida
Gastropoda
Crustacea
Actinia equina (one small specimen)
Gunda ulvae
Protodrilus flavocapitatus
Patella vulgata (very few)
Gammarus sp. (undescribed)
Melita palmata
Jaera marina
STATION L.
Coelenterata
Platyhelminthes
Gastropoda
Crustacea
Vertebrata
Actinia equina
Gunda ulvae (one specimen found on
one occasion only)
Craspedochilus cinereus
Patella vulgata
Gammarus sp. (undescribed)
Melita palmata
Jaera marina
Sphaeroma serratum
Carcinus maenas
Onos mustelus
STATION M.
As Station L; no Gunda found on any occasion.
The estimated population density of Gunda is shown in Fig. 1.
It will be seen that the fauna falls into well-defined regions:
I. The fresh-water fauna of the stream and pool. This usually ceases at P,
but during the calm weather and neap tides, July I5th-i6th, 1930, it extended
down to A.
II. A desert region devoid of fauna extending roughly from high-water level
of spring tides to high-water level of neap tides (Stations A-C).
III. A region containing only a poor fauna of Gunda, Protodrilus and an
Acoelan worm (only found July 15th, 1930). This region extends from high-water
neaps to the lower edge of the shingle (Stations C-E).
IV. A region containing Gunda, Protodrilus, Jaera and Gammarids (Stations
E-K), extending from the edge of the shingle to low-water neaps.
5-2
68
C. F. A. PANTIN
V. A region where a typical marine shore fauna is established, with Gunda'
absent, extending from just below low-water neaps out to sea.
Gunda occupies Regions III and IV.
The upper limit of the range of Gunda in Region III varies considerably.
During the calm weather and neap tides of July i5th-io,th, 1930, the range extended
to Station C, that is, to within a metre of high-water neap tide level. On the other
hand, during the rough weather and spring tides of July 28th-August 1st, 1930,
the desert region extended further down, and few Gunda were found even at
Station D.
This desert region is so striking that it merits discussion. The poverty and
variable limits of the fauna below this in Region III seem to be associated with the
fact that it is composed of shingle, which shifts in rough weather. The desert
region itself may lack a fauna, partly because of the intensity of mechanical disturbance to which it is subjected and, in the case of Gunda, because of the inconstant
bed of the stream at low tide. But these factors cannot completely account for the
absence of fauna, since Region III, which contains Gunda, is equally subject to
mechanical disturbance.
It is significant that this desert region corresponds roughly to the region
between high spring and high neap tides. Such a region which is only at long
intervals or irregularly subject to the presence of sea water is clearly a most
rigorous environment, and these conditions may well prevent encroachment of
Gunda into this region apart from the difficulties associated with mechanical
disturbance.
In the same way, the occasional incursions of sea water undoubtedly prevent
the fresh-water fauna from moving downwards. Thus, on July 19th, 1930, during
calm weather and neap tides, the fresh-water fauna had encroached on the desert
region down the stream below the pool, and was only limited at Station A, which
was below the level of high spring tides. By July 28th, 1930 (morning) the spring
tides and greater reaching power of the waves had driven the fresh-water fauna back
to the pool, P.
The evening tide of the same day was the highest of the month and the sea
was so rough that large .waves entered the pool at high tide. The fresh-water
fauna rapidly disappeared from the pool. By August 1st, 1930, however, the tides
were receding, the weather calmer, and the fresh-water fauna had re-established
itself in the upper half of the pool, the water of which was now fresh to the taste.
On its upper side the desert region thus seems to be defined by the tendency of
the fresh-water fauna to encroach downwards, the encroachment being limited by
incursions of sea water during high spring tides and rough weather. At other times,
particularly during neap tides, the downward movement is favoured by the fact
that at the upper edge of the tidal range the salinity may still be locally very low, and
is rapidly reduced as the tide retreats. Moreover, the fresh-water organisms can
withstand some concentration of sea water. Experiments on Polycelis cornuta
immersed for 24 hours in different dilutions of sea water showed that it could
withstand up to 6 per cent, of sea water for this period.
The Adaptation of Gunda ulvae to Salinity
69
But although some fresh-water organisms can withstand a small concentration
of sea water, and although some marine organisms such as Gunda can withstand
fresh water for a time, yet the desert region provides a real division between
what is only a modified marine fauna and what is a true fresh-water fauna. No
organisms were found which could not definitely be assigned to one or other of
these.
Throughout the rocky Region III Gunda is present in large numbers. The bed
of the stream here is permanent, depending on the shape of the rocks themselves.
Gunda ceases to be found within a few metres of low-water neap-tide
level: moderate numbers were found at Station K, but only one was found
on one occasion at Station L, 5 m. beyond. None were found at Station M.
This same limit was maintained both at neap tides and at the spring tides,
July 28th-August 1st, 1930. Salinity measurements indicate that the factor
in this case may be the insufficient dilution of the sea water by fresh water at
low tide.
It was remarkable that, although Protodrilus, which behaves in a manner similar
to Gunda with respect to salinity changes (Weil and Pantin, 1931), was found in
moderate numbers over almost exactly the same range as Gunda on July 15th19th, 1930, none of these were found at all on July 28th, 1930, and one near
low-water neaps on August 1st, 1930. Clearly some other unknown factor also
controls the distribution of Protodrilus. It must, therefore, be carefully borne in
mind that in Gunda itself factors not recognised in these papers may also control
its distribution, and that this description of its environment must be held to
apply rigidly only to the period when observations were made, the month of
July 1930.
SALINITY.
The salinity changes of the environment were determined by measurement of
the electric conductivity of the medium. Samples were taken over the region of the
distribution of Gunda. Their resistance was compared with artificial dilutions made
from one particular sample of sea water taken well clear of the stream mixed with
stream water taken about 300 yards inland. In comparison with this sample of
sea water English Channel sea water taken several miles from the coast had a
conductivity of 103 per cent. Since the water of the stream contains a large proportion of salts it has a fairly high conductivity, approximately equal to that
of a 0 7 per cent, solution of sea water in distilled water. With proper temperature
control the presence of o-oi per cent, of sea water in the river water can be
measured.
All measurements were made at 16-5° C.
The following observations show that the water in immediate contact with the
Gunda must vary from undiluted sea water to water in which the amount of sea
70
C.
F.
A.
PANTIN
water is negligible in comparison with the amount of salts already in the fresh
water.
July 15th, 1930.
STATION E.
Low tide: 3.30 p.m.
Sea water (%
0-03
3.30 p.m. Surface water
0-03
Under stone with Gunda ...
0-07
12 cm. below stone in shingle
High tide: 10.0 a.m.
12.20 p.m. (Station under 50 cm. of sea water
and 3-4 m. from water's edge)
100
Surface water
100
Under stone with Gunda ...
5 cm. below stone in shingle
95
The samples were taken by inserting a pipette under stones beneath which it
was supposed Gunda would be found, the presence of the latter being ascertained
after the sample was taken. The deep samples were taken in order to determine the
presence or absence of any water of very different salinity in the neighbourhood
of the Gunda.
Table II shows the successive changes in salinity during a single tide at six
stations down the estuary.
It is evident that the range covers enormous salinity variations. At the upper
end the worms are subject to a small percentage of sea water for perhaps an hour
each tide. At the lower end of the range they are under normal sea water for some
7 hours, and during the remaining 5 hours the sea water may fall to about 10 per
cent, of the normal concentration. In the maximal part of the range the salinity
varies from almost completely fresh water to undiluted sea water with each
tide.
It is apparent that Gunda is normally called upon to make full use of any
powers it has to withstand salinity changes. Indeed its occurrence becomes rare
as soon as these changes become reduced in magnitude (e.g. at Station L, just below
low-water neaps). This is remarkable because Gunda can be kept alive for months
in undiluted sea water, though experiments indicate (Pantin, 1931) that these conditions impair for a time their ability to withstand osmotic changes.
The general problem of adaptation to estuarine conditions is, therefore, presented in a most striking form by Gunda ulvae. A study of the physiological
mechanisms concerned in such a case as this may be expected to yield more information as to the means by which marine forms during evolution become adapted to
fresh-water existence than may be gleaned from most estuarine organisms, which
never come in contact with purely fresh water. Gunda can behave temporarily
as a fresh-water organism: why is it still sufficiently dependent upon sea water to
prevent its range extending into a purely fresh-water environment? In the succeeding papers an attempt is made to analyse the physiological changes induced
in the worms on transference from marine to fresh-water conditions.
The Adaptation of Gunda ulvae to Salinity
Table II.
High tide: 11.50 a.m.; 12.0 midnight. Low tide: 6.0 p.m. July 19th, 1930.
Station
Distance
below pool
(m.)
Height above
low-water
springs (m.)
C
165
43
D
230
38
Time
f.
h.
e.
10.30 a.m.
11.50
2.15 p.m.
1f.
f.
5-55
8.40
9.55 a.m.
f.
h.
E
G
K
L
33'O
460
78-0
84-0
30
2-4
17
1-2
10.40
11.45
e.
1.45 p.m.
e.
2.30
1f.
5-5°
8.40
f.
h.
e.
1f.
f.
10.15 a - m 11.50
2.40 p.m.
5-45
8.35
9.00
e.
e.
1f.
e.
e.
1 Je.
'if.
f.
e.
2.45 p.m.
3-iS
5-4°
8.30
3.30 p.m.
4-55
5-35
6.30
8.30
3.30 p.m.
Sea water (%) Sea water (%)
in surface
8 cm. in
shingle
water
o-oo
O'OI
3-2
0-16
003
000
001
o-oo
004
0-04
860
IOI-O
072
0-03
o-oo
O'OI
001
050
830
24-0
005
003
0-05
83-0
940
1030
IOO-O
3-i
3S-°
o-oi
o-oi
0-04
0-05
23-0
99°
92-0
25-0
91-0
280
0-56
90-0
73-o
870
ioo-o
IOO-O
260
43-0
67-0
6i-o
80
7-4
l.ff|f.
5.00
30
I"6.20
ioo-o
ioo-o
78-0
i.
8.30
6i-o
ioo-o
e.
001
139
IOO-O
IOO-O
090
720
810
IOO-O
C corresponded to the upper limit of Gunda.
D was in the shingle zone (III).
E on the upper border of the rock zone (IV).
G on the rock zone (IV).
K at the lower limit of Gunda, and
L 6 metres beyond K.
f.=flood; h. = high tide; e.=ebb; l.=low tide.
SUMMARY.
1. The environment of the triclad Gunda ulvae has been studied. This organism
lives on the sea shore in the estuaries of very small streams.
2. The components of the external medium are (a) stream water, which is rich
in Ca and C0 3 , and (b) Atlantic sea water. These are mixed in different proportions
in different parts of the estuary.
3. An analysis of the stream water is given.
4. The habitat of the organism is described. This extends roughly from highwater neap tides to low-water neap tides. A faunistic survey is given.
72
C. F. A. PANTIN
5. The conditions which control the limits of the habitat of Gunda are discussed.
Between the upper limit of occurrence of Gunda and the place of occurrence of
fresh-water forms there is a region devoid of fauna. This region corresponds roughly
with the span between high-water neap tides and high-water spring tides.
6. Salinity determinations have been made on samples taken from the actual
places where Gunda occurred. It is shown that Gunda has to withstand changes from
completely fresh to undiluted sea water. It may normally be exposed to either
extreme for several hours.
7. Salinity determinations made continually throughout the range of Gunda
show that its environment may vary from one in which it is subjected to the action
of sea water for only about 1 hour at high tide to one in which the sea water is only
diluted to about 10 per cent, of its normal strength for a few hours during low tide.
I wish to thank most gratefully Mr G. A. Steven of the Marine Biological
Laboratory, Plymouth, for his assistance in the identification of organisms, and
Mr M. A. Spender who very kindly surveyed the estuary of the stream for me.
I also wish to thank the Staff of the Marine Biological Laboratory, Plymouth, for
the many facilities with which I was provided.
REFERENCES.
DITTMAR, W. (1884). Challenger Report, Physics and Chemistry, 1, 203.
HUBAULT, E. (1927). Inverttbre's Torrenticoles. Paris: Dulau & Co.
PANTIN, C. F. A. (1931). Journ. Exp. Biol. 8, 82.
REID, D. M. (1930). Journ. Marine Biol. Assoc. 16, 609.
SCHLIEPER, C. (1929). Zeit.f. vergleich. Physiol. 9, 478.
THRESH, J. C. and BEALE, J. F. (1925). The Examination of Water and Water Supplies. 3rd ed.
London: J. and A. Churchill.
TREADWELL, F. P. and HALL, W. T. (1928). Analytical Chemistry, 2, 7th ed. John Wiley and Sons,
Inc.
WEIL, E. and PANTIN, C. F. A. (1931). Journ. Exp. Biol. 8, 73.
WHITEHEAD, H. (1921). Essex Naturalist, 20, 1.