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The burrowing and floating behaviour of the gastropod Hydrobia ulvae
Estuarine and Coastal Marine Science (1976) 4, 537-544
The Burrowing and Floating Behaviour of the Gastropod Hydrobia ulvae
Colin Little
and Wendy Nix
Department of Zoology, University of Bristol, Bristol BS8 IUG, England Received8 October1975and in revisedform 5 December1975
The behaviour of Hydrobia ulvae hasbeen investigatedat severallocalities on the British coast.No evidenceof rhythmic behaviourpatterns, previously postulatedfrom laboratory studies,hasbeen found. Floating appearsto be an accidental phenomenon,brought about by a variety of mechanisms. It may aid speciesdispersal.
Introduction Changesin behaviour related to the tidal cycle are common in littoral animals.While some of thesechangesare purely responsesto external stimuli, asfound in barnacles(Southward & Crisp, 1965),others have endogenouscomponents(e.g. Eurydice; seeJones& Naylor, 1970). Investigations of the estuarinegastropodHydrobia ulvae (Pennant) have suggestedthat both exogenous and endogenousfactors play a part in determining the behaviour exhibited throughout the tidal cycle (Newell, 1962). Since most of the observationsmadeon Hydrobia have been obtained in the laboratory, the present study was undertaken to observe the snail’sbehaviour in its natural environment in more detail. The observationsby Newell (1962) on the shorewest of Whitstable suggestedthat during the time of low tide an increasing proportion of the snails burrowed, but that the snails regained the surface of the mud immediately before the tide returned. Vader (1964), in contrast, reported that the snailssurfacedonly when actually submergedby the tide. Newell (1962) further stated that when the snailswere at the surfaceof the mud they floated actively on the water film just asthe tide wasabout to reachthem, and that a high, but undertermined, percentage of the animals remained afloat whilst the tide was flowing and ebbing. These observationson burrowing and floating are investigated further in the present paper.
Preliminary
observations
Burrowing Some brief observationswere first made at Gibraltar Point Nature Reserve,south of Skegnesson the eastcoastof England, which forms the northern boundary of the Wash. Observations were made from 6 to 27 July 1974. A transect was taken from MHWS towards low water, but since Hydrobia was mainly distributed around MHWN, no attempt was made to continue the transect down to low water. The animalswere separatedfrom the substratum by washingin a sieveof o*s-mmmeshbefore counting. Counts of the total population, including both buried and exposedindividuals, were madefirst. Then the snailson the surface of the mud were counted in adjacent areas,initially just after the tide had ebbed, and then again at 537
C. Little & W. Nix
low tide. During this period the percentage of buried snails increased greatly at all stations except 15 and 16 (Figure I). These two stations were exceptional in that they were located in a small depression containing water, the presence of which has been reported to inhibit burrowing (Linke, 1939). This supports the observations of Vader (rg64), but is in direct contrast to those reported by Newell (1962) who stated that the proportion of animals burrowing in sand covered by water was almost the same as that in sand and with no water film above. Observations in the salt marsh at Gibraltar Point showed that burrowing did not occur, presumably because the mud was too hard. As the area dried out, Hydrobia aggregated at the base of plant stems with the operculum closed, as also reported by Chatfield (1972). As might be expected, therefore, burrowing is far from being the only response to the withdrawal of water. Floating In order to estimate the numbers of floating snails as a percentage of the total population, a device consisting of four vertical poles connected by a metal framework, supporting a fine mesh net which enclosed an area of 25 x 25 cm, was employed. As the tide rose, snails floating
Height
O.D. (ml
3.6 1 (MHWS)
Stations
I
2.6 I
2
3
4
5
6
7
6
IOO-
2.0 I (MHWN)
9
IO
o-o-o
II
12
13
14
15
16
I7
-0 ‘0 ‘0
80 9: Buried 60-
40
.--0. I
-
-0
\
i
20 -
I :
Distance
\
\
0 l
\
\
I0 \ \ l --
/ d
I
I
I
50
60
70
(m)
Figure I. Distribution and burrowing behaviour of Hydmbia at Gibraltar Point. The upper kite diagram shows distribution after a spring tide of 3.6 m. The lower kite shows distribution after a tide of 2.6 m. Hatching represents mud and stippling represents sand. Where the two are combined, there was sand with superficial mud. The graph shows estimated percentage buried based on the numbers present on the surface at two times. 0, Counts made as the tide ebbed; Q, counts made at low tide.
Behaviour
of
Hydrobia ulvae
539
to the surface within the device were collected and retained. Counts were made of the total population in adjacent areas. The percentage of snails floating was recorded on two transects, one on the mud flat (Figure I) and the other on salt marsh. In both localities only a very small percentageof the population floated (Table I). No individuals were observed to turn upside down with an TABLE
I. The
Transect Tidal level EHWN
MHWN
percentage I (mud Station
of snails flat) % floating
10 II
0 0
I2
0
I3
0
I4
I5
0’20 0.25
16 I7
0 0
floating
at Gibraltar
Point
Transect 2 (salt marsh) Tidal % Station floating level EHWN
2
2A 3 3A
MHWN
2 5
0
0.24 o*rg 0’23 0.15 0’20 0
extended foot or to launch themselveson the incoming tide or on the water between ripple marks as describedby Newell (1962). Indeed, floating appearedto be passiveand the snails emergedonly when the shellswere already floating. This is in direct contrast to the observations of Newell, since he measuredthe specific gravity of Hydrobia and stated that neither adults nor young animalsused trapped air to float. In order to establishthat a wide cross-sectionof the population floated at Gibraltar Point, a sampleof floating snailswas collected at the edgeof the incoming tide asit moved over the salt marsh, using a fine meshsweepnet. The size compositionof a hundred snailsfrom this collection chosenat random is compared with a similar collection from the marsh surface in Figure 2. It is apparent that the young individuals were much more common in the population than on the marshsurface.
Figure 2. Size-frequency salt marsh at Gibraltar surface.
diagrams for IOO individuals collected at random from the Point. (a) floating snails. (b) snails collected from the marsh
540
C. Little & W. Nix
Further
observations
To investigate the variability of the behaviour of Hydrobiu, observations were made at a number of sitesin both winter and summer,as indicated below: BrancasterMarshes, Norfolk (grid ref. TF 804.445) Seasalter,near Whitstable, Kent (TR 055649) Calshot Spit, Southampton, Hams. (SU 487020) Weston-super-Mare, Somerset(ST 607314) Barry Harbour, South Glamorgan (ST 110667).
5OOi'-----
l -,-
---
.---
---
.v--*
1
---.
1
I
I
I
I
4
3
2
I
0
Time
before
coverage
by tide
(h)
Figure 3. Numbers of Hydrobia present on the mud surface at Barry recorded for 4 hr before cover by the tide. 0, Counts made on the mud pools; , counts on the adjacent open mud flat.
l
Harbour, surface in
Burrowing Initial inspection showedthat on all thesebeachesHydrobia remainedactive throughout the tidal cycle when covered with water, or when the mud surfaceremainedwet, but burrowed when the flat dried out. To confirm this, observationswere madeat Barry Harbour, in an area of fairly level mud flat, on 2 September 1975. In this area the density of Hydrobia was very uniform, and wassimilar in areasof damp mud and in areaswhere there were pools a few cm deep. Counts of animalson and just beneath the mud surfacewere 2900/m2in wet mud and 28oo/msin mud containing pools. From Figure 3 it can be seenthat for 4 hours before cover by the tide, the numbers crawling on the mud surface in the pools remained at 6o-75% of the population. On the exposedmud surface the numbers were already low when observation began, and they decreasedover the 4-hour period to approximately 5% of the total population. As the tide coveredthe flat, no snailswere seento cometo the surfaceof the mud, although those that were exposed on the mud surface soon becameactive when wetted. Vader (1964), working in the Netherlands, hasalsoshownthat surfacing occurred asa direct responseto water cover and that it did not occur before water reachedthe snailsassuggested by Newell (1962). Floating At the five siteslisted above, estimateswere madeof the percentageof the Hydrobia population which floated when the tide covered the mudflats, using similar methods to those
Behawiour
of Hydrobia
ulvae
541
describedfor Gibraltar Point. The catching device, however, wasenlargedto 0.25 m2and all counts of total populations were alsomade on this area. In generalthe region of maximum abundancewas located and the percentage floating there estimated. Detailed observations were alsomade on the mechanismsby which the snailscameto float on the surfacefilm. The results of theseobservationsare given in Table 2, together with somerelevant physical parameters. The percentagefloating ranged from o-6*20/Oand exceededI o/oonly in one instance. TABLE
Locality Brancaster Seasalter Calshot Weston
Barry
Tidal level MHWN MTLMHWN MLWN MTL
MTLMHWN Note:
2. The
percentage
Time (h)
Date 30 Dec. 74 12July 75 18 Feb. 75 II July 75 20 Dec. 74 30 July 75 IO Mar. 75 s May 75 22July 75 21 Aug. 75
*indicates
of the population
Salinity (%o S)
1s.o0*
20'0
20.30 13.00 12.00 13.00
17.3 9.0 29.8 31.0 32.8
15.00
15'5
14.00 17.00
27.0
15.00
18.00
that
it was after
29'4 28.0
floating Temperatore (“C) 4 17
8
23 9 29 13 I4 21 20
at five sites
Density (no./m”) 17 3oo 33 2oo 18000
No. floating per ma 72 2040 0
7300
“/b floating 0.42 6.15 0’00 0’00
6:
0.54
24
0.19
2700
0
0’00
1400 3100 2900
0 0
0’00 0’00
0
0’00
12500 12 700
dark.
On two occasions,the salinity of the inflowing water was lower than IO%,,, and such a dilution would be expected to reduce the activity of the snails (Newell, 1964). Very few floating Hydrobia were seenon the incoming tide at thesetimes and none were recorded in the observed quadrats, thus supporting Newell’s observationsin the River Crouch. Only one observation was made at night (Brancaster Marshes, 30 Dec. 1974). On this occasion0.4% of the population floated, and many snailswere seenon the incoming tide. Floating at night hasnot been previously recorded except in the laboratory (Anderson, 1971) and would not be predicted on the basisof Hydrobia’s responsesto light in the laboratory (Newell, 1962). No obvious correlation exists between the percentage floating and temperature which ranged from 4-29 “C during the observations. Unfortunately no measurementswere made below 4 “C becauseof the predominantly mild conditions in the winter of 1974/s. Closeobservationof the snailsas they were covered by the tide showedthat they cameto float in a variety of ways. These are dealt with in turn. Active mails. In wet mud, snailswere often active on the flats over the whole period during which they were uncovered. When the incoming tide produced small wavelets, many snails were rolled over to land with the aperture facing upwards. The foot was retracted slightly when this happenedand when it was extended again it often touched the surfacewater film becausethe tide had risen slightly. In this casethe film wastreated as a substratum and the snailscrawled upon it. snails. When the mud surface was fairly dry but conditions were not such as to impose a great degreeof desiccation, many snailswere often present on the mud surface. Their opercula were almost closed, but a slight gap was left between the edge of the operculum and the rim of the aperture. The majority had the aperture facing downwards and Inactive
542
C. Little & W. Nix
none of these floated. A few had the aperture facing upwards and as the water covered them, they extended the foot which contacted the surface film, upon which crawling then took place. At Brancaster, ten snails which were lying aperture-down were transferred to a position just above the incoming tide, with their apertures facing upwards. All these snails floated. Attempts to repeat this experiment at other times were only partially successful, however, and less than IOO~/~ of the transferred snails floated. Desiccated snails. Snails which climbed on to rocks and wooden groynes often became very desiccated, with the operculum well retracted. As the water flowed in over these objects, many snails were dislodged. They floated closed up on the surface film for approximately 15 s but then put out their tentacles and were crawling on the surface film within 30 s. Dried snails therefore do float and this is achieved by the use of the shell as a kind of ‘boat’. At this time the operculum is retracted far into the aperture and a large volume of air is present between the surface of the operculum and the rim of the upwards-facing aperture. Whether air is also present inside the mantle cavity has not been determined. Floating in ripple marks. This is the mechanism described by Newell (1962). Extensive searches have been made at all sites for snails floating in the water between ripple marks and in pools. Occasional individuals have been found at all stages of the tide at Weston, Calshot, Seasalter and Barry. At Seasalter many of these originated as desiccated specimens which were knocked off groynes or blown into the pools. On no occasion have the numbers floating been seen to increase just before the tide covered the pools. This is undoubtedly the least important floating mechanism. FZoating in the laboratory. Since such small percentages of snails were observed to float from the mudflats and since high percentages were observed by Newell (1962) to float in the laboratory, some comparisons were made of the populations observed on the shore with the same populations brought back to the laboratory. Great variability in the percentage floating in the laboratory was observed, as found previously by Newell. Between IO and 80% of the population floated, regardless of the area from which they were collected. Even when Hydrobia were collected from Weston, where the snails have never been observed to float on the tide, 50% of the population floated in the laboratory. As described by Newell, floating in the laboratory was influenced by light intensity and more snails floated when strong lights were used. Floating was also strongly dependent on the water depth. When the depth was greater than about I cm, snails rarely floated. This was because floating very seldom took place by the method of crawling up objects and then turning upside-down on the surface film as described by Newell. Almost all the snails that floated in the laboratory did so because they were placed aperture-upwards, and because the surface film was in reach of the foot when this was extended from the aperture. Since the percentages floating in the laboratory are so much greater than any observed in the field, the behaviour in the laboratory should probably be regarded as entirely artificial. Discussion A number of gastropod molluscs which rarely, if ever, float in nature will float in the laboratory, probably because they have better access to the surface water film and merely treat it as another convenient substratum. Personal observations have shown that Potamopyrgus (Hydrobia) jenkinsi floats in the laboratory, but this species is not known to float in its
Behviour
of Hydrobia ulvae
543
natural habitat. Similar observations apply to Rissoaparva, Lacuna pallid& and several nudibranchs including Polycera quadrilineata.The Limnaeidae float readily in aquaria, but they are also seenfloating on the water surface of the ponds in which they live (personal observations; seealsoCooke, 1913).Many marine molluscshave been seento employ ‘slime threads’ suspendedfrom the surface, on which they float (Colgan, agog), but it is most unlikely that such behaviour could occur naturally. The reasonswhy Hydrobia floats in its natural habitat have been the subject of speculationby a number of authors. Newell (1962) consideredthat the floating is geared to a rhythm and that it provides an additional substratum on which to feed. In the present study, no evidence hasbeen found for a rhythm in the natural populations of Hydrobia and sinceonly a very small proportion of the population floats, this idea does not seem particularly appropriate. It is possible that populations stranded on relatively clean sand, where little food is available,may be more active in their responseto the tide than those on mud flats. Populations on the sand at Weston, however, behave no differently from those on the mud. In view of this, the suggestionby Anderson (1971) that floating is an aid to dispersal,has more in its favour. In the Ythan estuary, Anderson has shown that the density of snailsfound on the ridges of solid objects on the mudflats, from which they might float on the incoming tide, was on averageonly approximately 16% of the density on the mud surface (calculated from data in Table I, Anderson, 1971). This suggeststhat contrary to Newell’s (1962) contention, the snailshave an innate tendency not to climb up objects. It may be, however, that the tendencieswithin the population are nicely balanced:the majority remainsburied and protected from desiccation,while a small proportion, at the risk of desiccation,is carried away by the tide, thus aiding in the dispersalof the species.Even so,this mechanismmust be an accessoryone, since it hasbeen shown by Fish & Fish (1974) that the veligers of Hydrobia swim actively and can be taken in plankton netsjust above the sedimentsurface,so that thesecould perfectly well bring about speciesdispersal. The mechanismsof floating describedhere amplify those describedby Anderson (1971). He showedthat desiccatedsnailssoonopenedwhen wetted by the tide, and crawled on the water surface. He alsoshowedthat dry Hydrobia could float, asfound in the present investigations. His observationsof small (lessthan 2 mm) specimensfloating up from the mud after being covered with water may explain the large percentageof juveniles found in the floating population at Gibraltar Point. The behaviour of Hydrobia in the Severn Estuary, at Weston and at Barry, is of interest becauseof the large tidal range and the associatedrapid rise of water level on the flood. If the snailsfloated in pools before the tide reached them, this rate of rise would make little difference to the percentagefloating; but since the snails are in fact activated by the tide water, they are not able to utilize the surface film before being completely submergedand little floating is observed. The rhythmic behaviour postulatedby Newell (1962)hasnot been seenat any of the sites visited in the present study. Vader (rg6q), in both field and laboratory observations, also failed to demonstrateany burrowing rhythm, and it seemsunlikely that a cycle as suggested by Newell could exist to any degree in the natural environment. It is more appropriate to conclude, asdid Newell for the majority of responsesshownby Hydrobia, that the behaviour of the snailsis governed by direct environmental stimuli. Acknowledgements We are grateful to Dr R. S. K. Barnes, Dr C. R. Boyden, Dr A. E. Dorey and Mrs P. E.
544
C. Little
&
W. Nix
Stirling for their comments and advice during this study, and for their assistance in the field. We also thank Dr T. E. Thompson for drawing our attention to the paper by Colgan.
References Anderson, A. 1971 Intertidal activity, breeding and the floating habit of Hydrobia ulvae in the Ythan estuary. ‘Journal of the Marine Biological Association of the United Kingdom 51, 423-437. Chatfield, J. E. 1972 Studies on variation and life history in the prosobranch Hydrobia ulvae (Pennant). Journal of Conchology 27,463-473. Colgan, N. 1909 Notes on locomotion and the use of slime threads in the marine Mollusca. Annals and Magazine of Natural History 3, 354-362. Cooke, A. H. 1913 Molluscs. In The Cambridge Natural History Vol. III (Harmer, S. F. & Shipley, A. E., eds). Macmillan, London. Fish, J. D. & Fish, S. 1974 The breeding cycle and growth of Hydrobia ulvae in the Dovey estuary. Journal of the Marine Biological Association of the United Kingdom 54, 685-697. Jones, D. A. & Naylor, E. 1970 The swimming rhythm of the sand beach isopod Eurydice pukhra. Journal of experimental marine Biology and Ecology 4, 188-199. Linke, 0. 1939 Die Biota des Jadebusenwattes. Helgollinder wissenschaftliche Meeresuntersuchungen I, 201-348. Newell R. 1962 Behavioural aspects of the ecology of Peringia (= Hydrobia) ulvae (Pennant) (Gasteropoda, Prosobranchia). Proceedings of the Zoological Society of London 138,49-75. Newell, R. 1964 Some factors controlling the upstream distribution of Hydrobia ulvae (Pennant), (Gastropoda, Prosobranchia). Proceedings of the Zoological Society of London 142, 85-106. Southward, A. J. & Crisp, D. J. 1965 Activity rhythms of barnacles in relation to respiration and feeding. Journal of the Marine Biological Association of the United Kingdom 45, 161-185. Vader, W. J. M. 1964 A preliminary investigation into the reactions of the infauna of the tidal flats to tidal fluctuations in water level. Netherlands Journal of Sea Research 2, 189-222.
The Burrowing and Floating Behaviour of the Gastropod Hydrobia ulvae
Colin Little
and Wendy Nix
Department of Zoology, University of Bristol, Bristol BS8 IUG, England Received8 October1975and in revisedform 5 December1975
The behaviour of Hydrobia ulvae hasbeen investigatedat severallocalities on the British coast.No evidenceof rhythmic behaviourpatterns, previously postulatedfrom laboratory studies,hasbeen found. Floating appearsto be an accidental phenomenon,brought about by a variety of mechanisms. It may aid speciesdispersal.
Introduction Changesin behaviour related to the tidal cycle are common in littoral animals.While some of thesechangesare purely responsesto external stimuli, asfound in barnacles(Southward & Crisp, 1965),others have endogenouscomponents(e.g. Eurydice; seeJones& Naylor, 1970). Investigations of the estuarinegastropodHydrobia ulvae (Pennant) have suggestedthat both exogenous and endogenousfactors play a part in determining the behaviour exhibited throughout the tidal cycle (Newell, 1962). Since most of the observationsmadeon Hydrobia have been obtained in the laboratory, the present study was undertaken to observe the snail’sbehaviour in its natural environment in more detail. The observationsby Newell (1962) on the shorewest of Whitstable suggestedthat during the time of low tide an increasing proportion of the snails burrowed, but that the snails regained the surface of the mud immediately before the tide returned. Vader (1964), in contrast, reported that the snailssurfacedonly when actually submergedby the tide. Newell (1962) further stated that when the snailswere at the surfaceof the mud they floated actively on the water film just asthe tide wasabout to reachthem, and that a high, but undertermined, percentage of the animals remained afloat whilst the tide was flowing and ebbing. These observationson burrowing and floating are investigated further in the present paper.
Preliminary
observations
Burrowing Some brief observationswere first made at Gibraltar Point Nature Reserve,south of Skegnesson the eastcoastof England, which forms the northern boundary of the Wash. Observations were made from 6 to 27 July 1974. A transect was taken from MHWS towards low water, but since Hydrobia was mainly distributed around MHWN, no attempt was made to continue the transect down to low water. The animalswere separatedfrom the substratum by washingin a sieveof o*s-mmmeshbefore counting. Counts of the total population, including both buried and exposedindividuals, were madefirst. Then the snailson the surface of the mud were counted in adjacent areas,initially just after the tide had ebbed, and then again at 537
C. Little & W. Nix
low tide. During this period the percentage of buried snails increased greatly at all stations except 15 and 16 (Figure I). These two stations were exceptional in that they were located in a small depression containing water, the presence of which has been reported to inhibit burrowing (Linke, 1939). This supports the observations of Vader (rg64), but is in direct contrast to those reported by Newell (1962) who stated that the proportion of animals burrowing in sand covered by water was almost the same as that in sand and with no water film above. Observations in the salt marsh at Gibraltar Point showed that burrowing did not occur, presumably because the mud was too hard. As the area dried out, Hydrobia aggregated at the base of plant stems with the operculum closed, as also reported by Chatfield (1972). As might be expected, therefore, burrowing is far from being the only response to the withdrawal of water. Floating In order to estimate the numbers of floating snails as a percentage of the total population, a device consisting of four vertical poles connected by a metal framework, supporting a fine mesh net which enclosed an area of 25 x 25 cm, was employed. As the tide rose, snails floating
Height
O.D. (ml
3.6 1 (MHWS)
Stations
I
2.6 I
2
3
4
5
6
7
6
IOO-
2.0 I (MHWN)
9
IO
o-o-o
II
12
13
14
15
16
I7
-0 ‘0 ‘0
80 9: Buried 60-
40
.--0. I
-
-0
\
i
20 -
I :
Distance
\
\
0 l
\
\
I0 \ \ l --
/ d
I
I
I
50
60
70
(m)
Figure I. Distribution and burrowing behaviour of Hydmbia at Gibraltar Point. The upper kite diagram shows distribution after a spring tide of 3.6 m. The lower kite shows distribution after a tide of 2.6 m. Hatching represents mud and stippling represents sand. Where the two are combined, there was sand with superficial mud. The graph shows estimated percentage buried based on the numbers present on the surface at two times. 0, Counts made as the tide ebbed; Q, counts made at low tide.
Behaviour
of
Hydrobia ulvae
539
to the surface within the device were collected and retained. Counts were made of the total population in adjacent areas. The percentage of snails floating was recorded on two transects, one on the mud flat (Figure I) and the other on salt marsh. In both localities only a very small percentageof the population floated (Table I). No individuals were observed to turn upside down with an TABLE
I. The
Transect Tidal level EHWN
MHWN
percentage I (mud Station
of snails flat) % floating
10 II
0 0
I2
0
I3
0
I4
I5
0’20 0.25
16 I7
0 0
floating
at Gibraltar
Point
Transect 2 (salt marsh) Tidal % Station floating level EHWN
2
2A 3 3A
MHWN
2 5
0
0.24 o*rg 0’23 0.15 0’20 0
extended foot or to launch themselveson the incoming tide or on the water between ripple marks as describedby Newell (1962). Indeed, floating appearedto be passiveand the snails emergedonly when the shellswere already floating. This is in direct contrast to the observations of Newell, since he measuredthe specific gravity of Hydrobia and stated that neither adults nor young animalsused trapped air to float. In order to establishthat a wide cross-sectionof the population floated at Gibraltar Point, a sampleof floating snailswas collected at the edgeof the incoming tide asit moved over the salt marsh, using a fine meshsweepnet. The size compositionof a hundred snailsfrom this collection chosenat random is compared with a similar collection from the marsh surface in Figure 2. It is apparent that the young individuals were much more common in the population than on the marshsurface.
Figure 2. Size-frequency salt marsh at Gibraltar surface.
diagrams for IOO individuals collected at random from the Point. (a) floating snails. (b) snails collected from the marsh
540
C. Little & W. Nix
Further
observations
To investigate the variability of the behaviour of Hydrobiu, observations were made at a number of sitesin both winter and summer,as indicated below: BrancasterMarshes, Norfolk (grid ref. TF 804.445) Seasalter,near Whitstable, Kent (TR 055649) Calshot Spit, Southampton, Hams. (SU 487020) Weston-super-Mare, Somerset(ST 607314) Barry Harbour, South Glamorgan (ST 110667).
5OOi'-----
l -,-
---
.---
---
.v--*
1
---.
1
I
I
I
I
4
3
2
I
0
Time
before
coverage
by tide
(h)
Figure 3. Numbers of Hydrobia present on the mud surface at Barry recorded for 4 hr before cover by the tide. 0, Counts made on the mud pools; , counts on the adjacent open mud flat.
l
Harbour, surface in
Burrowing Initial inspection showedthat on all thesebeachesHydrobia remainedactive throughout the tidal cycle when covered with water, or when the mud surfaceremainedwet, but burrowed when the flat dried out. To confirm this, observationswere madeat Barry Harbour, in an area of fairly level mud flat, on 2 September 1975. In this area the density of Hydrobia was very uniform, and wassimilar in areasof damp mud and in areaswhere there were pools a few cm deep. Counts of animalson and just beneath the mud surfacewere 2900/m2in wet mud and 28oo/msin mud containing pools. From Figure 3 it can be seenthat for 4 hours before cover by the tide, the numbers crawling on the mud surface in the pools remained at 6o-75% of the population. On the exposedmud surface the numbers were already low when observation began, and they decreasedover the 4-hour period to approximately 5% of the total population. As the tide coveredthe flat, no snailswere seento cometo the surfaceof the mud, although those that were exposed on the mud surface soon becameactive when wetted. Vader (1964), working in the Netherlands, hasalsoshownthat surfacing occurred asa direct responseto water cover and that it did not occur before water reachedthe snailsassuggested by Newell (1962). Floating At the five siteslisted above, estimateswere madeof the percentageof the Hydrobia population which floated when the tide covered the mudflats, using similar methods to those
Behawiour
of Hydrobia
ulvae
541
describedfor Gibraltar Point. The catching device, however, wasenlargedto 0.25 m2and all counts of total populations were alsomade on this area. In generalthe region of maximum abundancewas located and the percentage floating there estimated. Detailed observations were alsomade on the mechanismsby which the snailscameto float on the surfacefilm. The results of theseobservationsare given in Table 2, together with somerelevant physical parameters. The percentagefloating ranged from o-6*20/Oand exceededI o/oonly in one instance. TABLE
Locality Brancaster Seasalter Calshot Weston
Barry
Tidal level MHWN MTLMHWN MLWN MTL
MTLMHWN Note:
2. The
percentage
Time (h)
Date 30 Dec. 74 12July 75 18 Feb. 75 II July 75 20 Dec. 74 30 July 75 IO Mar. 75 s May 75 22July 75 21 Aug. 75
*indicates
of the population
Salinity (%o S)
1s.o0*
20'0
20.30 13.00 12.00 13.00
17.3 9.0 29.8 31.0 32.8
15.00
15'5
14.00 17.00
27.0
15.00
18.00
that
it was after
29'4 28.0
floating Temperatore (“C) 4 17
8
23 9 29 13 I4 21 20
at five sites
Density (no./m”) 17 3oo 33 2oo 18000
No. floating per ma 72 2040 0
7300
“/b floating 0.42 6.15 0’00 0’00
6:
0.54
24
0.19
2700
0
0’00
1400 3100 2900
0 0
0’00 0’00
0
0’00
12500 12 700
dark.
On two occasions,the salinity of the inflowing water was lower than IO%,,, and such a dilution would be expected to reduce the activity of the snails (Newell, 1964). Very few floating Hydrobia were seenon the incoming tide at thesetimes and none were recorded in the observed quadrats, thus supporting Newell’s observationsin the River Crouch. Only one observation was made at night (Brancaster Marshes, 30 Dec. 1974). On this occasion0.4% of the population floated, and many snailswere seenon the incoming tide. Floating at night hasnot been previously recorded except in the laboratory (Anderson, 1971) and would not be predicted on the basisof Hydrobia’s responsesto light in the laboratory (Newell, 1962). No obvious correlation exists between the percentage floating and temperature which ranged from 4-29 “C during the observations. Unfortunately no measurementswere made below 4 “C becauseof the predominantly mild conditions in the winter of 1974/s. Closeobservationof the snailsas they were covered by the tide showedthat they cameto float in a variety of ways. These are dealt with in turn. Active mails. In wet mud, snailswere often active on the flats over the whole period during which they were uncovered. When the incoming tide produced small wavelets, many snails were rolled over to land with the aperture facing upwards. The foot was retracted slightly when this happenedand when it was extended again it often touched the surfacewater film becausethe tide had risen slightly. In this casethe film wastreated as a substratum and the snailscrawled upon it. snails. When the mud surface was fairly dry but conditions were not such as to impose a great degreeof desiccation, many snailswere often present on the mud surface. Their opercula were almost closed, but a slight gap was left between the edge of the operculum and the rim of the aperture. The majority had the aperture facing downwards and Inactive
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none of these floated. A few had the aperture facing upwards and as the water covered them, they extended the foot which contacted the surface film, upon which crawling then took place. At Brancaster, ten snails which were lying aperture-down were transferred to a position just above the incoming tide, with their apertures facing upwards. All these snails floated. Attempts to repeat this experiment at other times were only partially successful, however, and less than IOO~/~ of the transferred snails floated. Desiccated snails. Snails which climbed on to rocks and wooden groynes often became very desiccated, with the operculum well retracted. As the water flowed in over these objects, many snails were dislodged. They floated closed up on the surface film for approximately 15 s but then put out their tentacles and were crawling on the surface film within 30 s. Dried snails therefore do float and this is achieved by the use of the shell as a kind of ‘boat’. At this time the operculum is retracted far into the aperture and a large volume of air is present between the surface of the operculum and the rim of the upwards-facing aperture. Whether air is also present inside the mantle cavity has not been determined. Floating in ripple marks. This is the mechanism described by Newell (1962). Extensive searches have been made at all sites for snails floating in the water between ripple marks and in pools. Occasional individuals have been found at all stages of the tide at Weston, Calshot, Seasalter and Barry. At Seasalter many of these originated as desiccated specimens which were knocked off groynes or blown into the pools. On no occasion have the numbers floating been seen to increase just before the tide covered the pools. This is undoubtedly the least important floating mechanism. FZoating in the laboratory. Since such small percentages of snails were observed to float from the mudflats and since high percentages were observed by Newell (1962) to float in the laboratory, some comparisons were made of the populations observed on the shore with the same populations brought back to the laboratory. Great variability in the percentage floating in the laboratory was observed, as found previously by Newell. Between IO and 80% of the population floated, regardless of the area from which they were collected. Even when Hydrobia were collected from Weston, where the snails have never been observed to float on the tide, 50% of the population floated in the laboratory. As described by Newell, floating in the laboratory was influenced by light intensity and more snails floated when strong lights were used. Floating was also strongly dependent on the water depth. When the depth was greater than about I cm, snails rarely floated. This was because floating very seldom took place by the method of crawling up objects and then turning upside-down on the surface film as described by Newell. Almost all the snails that floated in the laboratory did so because they were placed aperture-upwards, and because the surface film was in reach of the foot when this was extended from the aperture. Since the percentages floating in the laboratory are so much greater than any observed in the field, the behaviour in the laboratory should probably be regarded as entirely artificial. Discussion A number of gastropod molluscs which rarely, if ever, float in nature will float in the laboratory, probably because they have better access to the surface water film and merely treat it as another convenient substratum. Personal observations have shown that Potamopyrgus (Hydrobia) jenkinsi floats in the laboratory, but this species is not known to float in its
Behviour
of Hydrobia ulvae
543
natural habitat. Similar observations apply to Rissoaparva, Lacuna pallid& and several nudibranchs including Polycera quadrilineata.The Limnaeidae float readily in aquaria, but they are also seenfloating on the water surface of the ponds in which they live (personal observations; seealsoCooke, 1913).Many marine molluscshave been seento employ ‘slime threads’ suspendedfrom the surface, on which they float (Colgan, agog), but it is most unlikely that such behaviour could occur naturally. The reasonswhy Hydrobia floats in its natural habitat have been the subject of speculationby a number of authors. Newell (1962) consideredthat the floating is geared to a rhythm and that it provides an additional substratum on which to feed. In the present study, no evidence hasbeen found for a rhythm in the natural populations of Hydrobia and sinceonly a very small proportion of the population floats, this idea does not seem particularly appropriate. It is possible that populations stranded on relatively clean sand, where little food is available,may be more active in their responseto the tide than those on mud flats. Populations on the sand at Weston, however, behave no differently from those on the mud. In view of this, the suggestionby Anderson (1971) that floating is an aid to dispersal,has more in its favour. In the Ythan estuary, Anderson has shown that the density of snailsfound on the ridges of solid objects on the mudflats, from which they might float on the incoming tide, was on averageonly approximately 16% of the density on the mud surface (calculated from data in Table I, Anderson, 1971). This suggeststhat contrary to Newell’s (1962) contention, the snailshave an innate tendency not to climb up objects. It may be, however, that the tendencieswithin the population are nicely balanced:the majority remainsburied and protected from desiccation,while a small proportion, at the risk of desiccation,is carried away by the tide, thus aiding in the dispersalof the species.Even so,this mechanismmust be an accessoryone, since it hasbeen shown by Fish & Fish (1974) that the veligers of Hydrobia swim actively and can be taken in plankton netsjust above the sedimentsurface,so that thesecould perfectly well bring about speciesdispersal. The mechanismsof floating describedhere amplify those describedby Anderson (1971). He showedthat desiccatedsnailssoonopenedwhen wetted by the tide, and crawled on the water surface. He alsoshowedthat dry Hydrobia could float, asfound in the present investigations. His observationsof small (lessthan 2 mm) specimensfloating up from the mud after being covered with water may explain the large percentageof juveniles found in the floating population at Gibraltar Point. The behaviour of Hydrobia in the Severn Estuary, at Weston and at Barry, is of interest becauseof the large tidal range and the associatedrapid rise of water level on the flood. If the snailsfloated in pools before the tide reached them, this rate of rise would make little difference to the percentagefloating; but since the snails are in fact activated by the tide water, they are not able to utilize the surface film before being completely submergedand little floating is observed. The rhythmic behaviour postulatedby Newell (1962)hasnot been seenat any of the sites visited in the present study. Vader (rg6q), in both field and laboratory observations, also failed to demonstrateany burrowing rhythm, and it seemsunlikely that a cycle as suggested by Newell could exist to any degree in the natural environment. It is more appropriate to conclude, asdid Newell for the majority of responsesshownby Hydrobia, that the behaviour of the snailsis governed by direct environmental stimuli. Acknowledgements We are grateful to Dr R. S. K. Barnes, Dr C. R. Boyden, Dr A. E. Dorey and Mrs P. E.
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Stirling for their comments and advice during this study, and for their assistance in the field. We also thank Dr T. E. Thompson for drawing our attention to the paper by Colgan.
References Anderson, A. 1971 Intertidal activity, breeding and the floating habit of Hydrobia ulvae in the Ythan estuary. ‘Journal of the Marine Biological Association of the United Kingdom 51, 423-437. Chatfield, J. E. 1972 Studies on variation and life history in the prosobranch Hydrobia ulvae (Pennant). Journal of Conchology 27,463-473. Colgan, N. 1909 Notes on locomotion and the use of slime threads in the marine Mollusca. Annals and Magazine of Natural History 3, 354-362. Cooke, A. H. 1913 Molluscs. In The Cambridge Natural History Vol. III (Harmer, S. F. & Shipley, A. E., eds). Macmillan, London. Fish, J. D. & Fish, S. 1974 The breeding cycle and growth of Hydrobia ulvae in the Dovey estuary. Journal of the Marine Biological Association of the United Kingdom 54, 685-697. Jones, D. A. & Naylor, E. 1970 The swimming rhythm of the sand beach isopod Eurydice pukhra. Journal of experimental marine Biology and Ecology 4, 188-199. Linke, 0. 1939 Die Biota des Jadebusenwattes. Helgollinder wissenschaftliche Meeresuntersuchungen I, 201-348. Newell R. 1962 Behavioural aspects of the ecology of Peringia (= Hydrobia) ulvae (Pennant) (Gasteropoda, Prosobranchia). Proceedings of the Zoological Society of London 138,49-75. Newell, R. 1964 Some factors controlling the upstream distribution of Hydrobia ulvae (Pennant), (Gastropoda, Prosobranchia). Proceedings of the Zoological Society of London 142, 85-106. Southward, A. J. & Crisp, D. J. 1965 Activity rhythms of barnacles in relation to respiration and feeding. Journal of the Marine Biological Association of the United Kingdom 45, 161-185. Vader, W. J. M. 1964 A preliminary investigation into the reactions of the infauna of the tidal flats to tidal fluctuations in water level. Netherlands Journal of Sea Research 2, 189-222.