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Crawling-tracks of trematode infected Macoma balthica (L.)
Netherlands Journal of Sea Research 4 (3): 376-379 (1969)
CRAWLING-TRACKS OF TREMATODE INFECTED MACOMA BALTHICA (L.' by C.
SWENNEN
(Netherlands Institutefor Sea Research, Den Helder, The Netherlands)
CONTENTS I. II. Iti. IV.
Introduction Observations Discuasion Summary References
376 376 378 379 379
.
I. I N T R O D U C T I O N The small bivalve mollusc Maxoma balthka (Linnaeus, 1758) has many predators, chiefly among birds and fishes. For a predator, however, it is presumably not easily located. The animals live dispersed and burrowed into the sea bottom so that they are hidden from view. Therefore it is remarkable that in many places on the Dutch coast and also elsewhere along the North Sea (MoRTENS~N, 1922:41; HAGmSmR & K ~ D t ~ r t , 1927:8; B~FmLD & NEWELL, 1961) now and again individuals were observed which had made very conspicuous crawling-trails on the sand of the tidal area, thereby clearly indicating their position. Macoma tracks have been associated with foraging activities (B~,FmLD & NEWELL, 1961), with moving to a lower level in the tidal zone after having been covered with sand in rough weather (HAOI~tER & K~xsNDLER,1927), and also with prospecting for places with a more favourable oxygen content (BRArmra), I963). In this paper it will be demonstrated that there is a connection between the trails and parasitization of Mazoma by a trematode. I would like to thank Mr. M. Eelman o f the State Forestry on Texel for providing the duetdings used and Miss S. M. van der Baan for translating the manuscript. II. O B S E R V A T I O N S The furrows in the substratum (Plate I) are caused by crawling of Macoma batthica in a horizontal direction on the sands which emerge at
Crawling-trails of
i~lacoma balthica oil
PLATE I sandy tidal flat, Terschelling, Boschplaat, April 1958,
PLATE
II
Fig. 1. Macoma balthica collected from crawllng-trai]. One valve is removed. Body filled with white cysts of a Gymnophallid trematode.
1 Fig. 2. Transverse section through 3/lacoma from crawling-trail. Except for muscle tissue and digestive tract the whole body is filled with metacercariae in sporocysts.
CRAWLING-TRACKS OF MACOMA BALTHICA
377
lOW tide. Such traces were found in the following localities along the Dutch coast: Terschelling: tidal flats along the Boschplaat and along the Noordsvaarder, Vlieland: on the Kichel and the Posthuiswad, Texel: in the Slufter and the Mokbaai, Den Helder: on the Zuidwal and the Balgzand, Wieringen: tidal flats at the Normert, Hoek van Holland: beach of Rozenburg, Voorne: mouth of the Brielse Maas. In all cases the bottom consisted of sand mixed with a certain amount of mud, except for the Brielse Maas, where the bottom was of pure mud. At all these localities trails of Macoma were only observed in the higher parts of the littoral, from mid-tide level upwards. The trails were found from December till the end of May, but they were most numerous in early spring. The phenomenon may be less conspicuous in one year than in the next. The furrowing animals can be found at the end of their trail, just under the surface. Their position is often marked by a slight elevation of the surface; they can therefore easily be located by sight. With their valves closed these individuals are similar to the other, stationary animals, but when one of the valves is removed it is visible even to the naked eye that they are filled with sausage-shaped objects (Plate II fig. 1), which on closer examination turn out to be sporocysts, containing scores of metacercariae. So far the exact species could not be identified; however, it belongs to the family Gymnophallidae (Trematoda). At all the above-named localities along the Dutch coast these sporocysts were found in every Macoma, collected at the end of a crawlingtrail. At some of these localities Macoma's were also collected by sieving bottom samples. It turned out that, per unit surface area, there are over a hundred times as many Macoma specimens as trails, and also TABLE
I
Percentage of sporocyst infection in animals collected from trails, compared with specimens collected at random in the same area. Locality
Terschelling
Texel
*
x~_test.
Date
April 1955
April 1968
Number of Macoma examined
Number containingsporocysts
from trails 28
28
at random 52
7
from trails 49
49
at random 110
6
I00% P<0.001* 13% 100% P<0.001* 5%
378
c. SWENNEN
that specimens from bottom samples had a significantly lower pc~:.... centage containing sporocysts (Table I). In numerous samples from lower levels in the littoral--where cra~ ling-trails were never o b s e r v e d - - a n d from the sublittoral a Macoma with sporocysts was only exceptionally found. There is no clear difl~:-ence between the specimens as to the intensity of infection, in all i~fected animals the whole of the body, except for the muscles and some essential organs, turned out to be completely filled with sporocysts (Plate I I fig. 2). Infection experiments with uninfected newly-hatched ducklings (Anas platyrhynchos) showed that the metacercariae from sporocysts in Macoma developed into mature flukes in the ducklings in the course of one single day. In Macoma, however, the metacercariae stayed in lhe same stage of development for months on end.
III. D I S C U S S I O N The specimens of Macoma balthica which make furrows in the surface of the tidal flats at tow tide are remarkable because as a rule this species does not leave the slightest indication of its position. Macoma lives burrowed to a depth between 1 and 12 era, and the animals are practically randomly dispersed. The contact with the above-lying water and the surface of the sediment is maintained by long, thin siphons, of which one m a y be stretched out considerably when the animal searches for food. These siphons are hyaline and therefore not conspicuous. When disturbed the animal retracts them quickly and as their diameter is very small they usually leave no hole in the substratum. The animal feeds on the deposit at the surface, but traces of feeding as described by THAMDRUP (1935: 46) are only visible at exceptional conditions. As a rule it is certainly not a prey which can be easily traced by a predator. Birds, such as oystercatchers (HuLserIER, 1964) as well as curlew, bar-tailed godwit, knot, herring gull, shetduck and eider Iown unpublished data from examination of faeces and pellets), prey on Macoma. As a rule birds find their prey by sight. Experiments with caged dunlins and oystercatehers as well as field observations indicate that even the waders, though quite capable to find their prey by tactile sense, are often directed by visible traces when boring for prey. To a furrowing Macoma the risk of predation must be very much greater. In all previous observations the stimulus for crawling behaviour at low tide was supposed to be a negative environmental factor, such as too much sand, lack of food or lack of oxygen. For Macoma the act of crawling at low tide seems to involve a waste of energy and to increase
C R A W L I N G - T R A C K S OF MACOMA B A L T H I C A
379
the risk of predation. For the parasite, however, it is essential that its host is eaten by a bird, thus enabling the fluke to complete its life-cycle. Since a much higher percentage of crawling Macoma specimens is infected than is the case with the stationary, usually deeply burrowed animals, it seems likely that the sporocysts form the stimulus which induces Macoma to crawl on the surface of the tidal flats.
IV. S U M M A R Y
At higher levels in the tidal zone conspicuous crawling-trails of Macoma balthica are sometimes found. The specimens making these trails turned out to be filled with sporocysts of an as yet unidentified Gymnophallid trematode. It was proved that the parasite does not develop any further in the mollusc, but that in a bird the sexually mature stage is reached within 24 hours. It is supposed that the parasite stimulates the host to crawling behaviour, thus increasing the chance of predation by a bird.
REFERENCES
BRAFIELD,A. E., 1963. The effects of oxygen deficiency on the behaviour of Macoma balthica (L.).--Anim. Behav. U (2-3): 345-346. BRAFIELD, A. E. & G. E. NEWZLL, 1961. The behaviour of Macoma balthica (L.).-J. Mar. biol. Ass. U.K. 44: 81-87. HAGMEmR, A. & R. KKNDLER, 1927. Neue Untersuchungen im nordfriesischen Wattenmeer und auf den fiskalischen Austerb~inken.--Wiss. Meeresunters., Helgoland 16: 1-90. HULSCHER, J. B., 1964. Scholeksters en larnellibranchiaten in de Waddenzee.-Levende Nat. 67: 80-85. MORa~NS~N, T., 1922. Biologiske Studier over Sandstrandsfaunaen, smrlig ved de danske Kyster.--Vidensk. Meddr dansk naturh. Foren. 74: 23-57. THAMDRUP, H. M., 1935. Beitr~ige zur Oekologie der Wattenfauna. Meddr Kommn Havunders., Fiskeri 10 (2): 1-125.
25
CRAWLING-TRACKS OF TREMATODE INFECTED MACOMA BALTHICA (L.' by C.
SWENNEN
(Netherlands Institutefor Sea Research, Den Helder, The Netherlands)
CONTENTS I. II. Iti. IV.
Introduction Observations Discuasion Summary References
376 376 378 379 379
.
I. I N T R O D U C T I O N The small bivalve mollusc Maxoma balthka (Linnaeus, 1758) has many predators, chiefly among birds and fishes. For a predator, however, it is presumably not easily located. The animals live dispersed and burrowed into the sea bottom so that they are hidden from view. Therefore it is remarkable that in many places on the Dutch coast and also elsewhere along the North Sea (MoRTENS~N, 1922:41; HAGmSmR & K ~ D t ~ r t , 1927:8; B~FmLD & NEWELL, 1961) now and again individuals were observed which had made very conspicuous crawling-trails on the sand of the tidal area, thereby clearly indicating their position. Macoma tracks have been associated with foraging activities (B~,FmLD & NEWELL, 1961), with moving to a lower level in the tidal zone after having been covered with sand in rough weather (HAOI~tER & K~xsNDLER,1927), and also with prospecting for places with a more favourable oxygen content (BRArmra), I963). In this paper it will be demonstrated that there is a connection between the trails and parasitization of Mazoma by a trematode. I would like to thank Mr. M. Eelman o f the State Forestry on Texel for providing the duetdings used and Miss S. M. van der Baan for translating the manuscript. II. O B S E R V A T I O N S The furrows in the substratum (Plate I) are caused by crawling of Macoma batthica in a horizontal direction on the sands which emerge at
Crawling-trails of
i~lacoma balthica oil
PLATE I sandy tidal flat, Terschelling, Boschplaat, April 1958,
PLATE
II
Fig. 1. Macoma balthica collected from crawllng-trai]. One valve is removed. Body filled with white cysts of a Gymnophallid trematode.
1 Fig. 2. Transverse section through 3/lacoma from crawling-trail. Except for muscle tissue and digestive tract the whole body is filled with metacercariae in sporocysts.
CRAWLING-TRACKS OF MACOMA BALTHICA
377
lOW tide. Such traces were found in the following localities along the Dutch coast: Terschelling: tidal flats along the Boschplaat and along the Noordsvaarder, Vlieland: on the Kichel and the Posthuiswad, Texel: in the Slufter and the Mokbaai, Den Helder: on the Zuidwal and the Balgzand, Wieringen: tidal flats at the Normert, Hoek van Holland: beach of Rozenburg, Voorne: mouth of the Brielse Maas. In all cases the bottom consisted of sand mixed with a certain amount of mud, except for the Brielse Maas, where the bottom was of pure mud. At all these localities trails of Macoma were only observed in the higher parts of the littoral, from mid-tide level upwards. The trails were found from December till the end of May, but they were most numerous in early spring. The phenomenon may be less conspicuous in one year than in the next. The furrowing animals can be found at the end of their trail, just under the surface. Their position is often marked by a slight elevation of the surface; they can therefore easily be located by sight. With their valves closed these individuals are similar to the other, stationary animals, but when one of the valves is removed it is visible even to the naked eye that they are filled with sausage-shaped objects (Plate II fig. 1), which on closer examination turn out to be sporocysts, containing scores of metacercariae. So far the exact species could not be identified; however, it belongs to the family Gymnophallidae (Trematoda). At all the above-named localities along the Dutch coast these sporocysts were found in every Macoma, collected at the end of a crawlingtrail. At some of these localities Macoma's were also collected by sieving bottom samples. It turned out that, per unit surface area, there are over a hundred times as many Macoma specimens as trails, and also TABLE
I
Percentage of sporocyst infection in animals collected from trails, compared with specimens collected at random in the same area. Locality
Terschelling
Texel
*
x~_test.
Date
April 1955
April 1968
Number of Macoma examined
Number containingsporocysts
from trails 28
28
at random 52
7
from trails 49
49
at random 110
6
I00% P<0.001* 13% 100% P<0.001* 5%
378
c. SWENNEN
that specimens from bottom samples had a significantly lower pc~:.... centage containing sporocysts (Table I). In numerous samples from lower levels in the littoral--where cra~ ling-trails were never o b s e r v e d - - a n d from the sublittoral a Macoma with sporocysts was only exceptionally found. There is no clear difl~:-ence between the specimens as to the intensity of infection, in all i~fected animals the whole of the body, except for the muscles and some essential organs, turned out to be completely filled with sporocysts (Plate I I fig. 2). Infection experiments with uninfected newly-hatched ducklings (Anas platyrhynchos) showed that the metacercariae from sporocysts in Macoma developed into mature flukes in the ducklings in the course of one single day. In Macoma, however, the metacercariae stayed in lhe same stage of development for months on end.
III. D I S C U S S I O N The specimens of Macoma balthica which make furrows in the surface of the tidal flats at tow tide are remarkable because as a rule this species does not leave the slightest indication of its position. Macoma lives burrowed to a depth between 1 and 12 era, and the animals are practically randomly dispersed. The contact with the above-lying water and the surface of the sediment is maintained by long, thin siphons, of which one m a y be stretched out considerably when the animal searches for food. These siphons are hyaline and therefore not conspicuous. When disturbed the animal retracts them quickly and as their diameter is very small they usually leave no hole in the substratum. The animal feeds on the deposit at the surface, but traces of feeding as described by THAMDRUP (1935: 46) are only visible at exceptional conditions. As a rule it is certainly not a prey which can be easily traced by a predator. Birds, such as oystercatchers (HuLserIER, 1964) as well as curlew, bar-tailed godwit, knot, herring gull, shetduck and eider Iown unpublished data from examination of faeces and pellets), prey on Macoma. As a rule birds find their prey by sight. Experiments with caged dunlins and oystercatehers as well as field observations indicate that even the waders, though quite capable to find their prey by tactile sense, are often directed by visible traces when boring for prey. To a furrowing Macoma the risk of predation must be very much greater. In all previous observations the stimulus for crawling behaviour at low tide was supposed to be a negative environmental factor, such as too much sand, lack of food or lack of oxygen. For Macoma the act of crawling at low tide seems to involve a waste of energy and to increase
C R A W L I N G - T R A C K S OF MACOMA B A L T H I C A
379
the risk of predation. For the parasite, however, it is essential that its host is eaten by a bird, thus enabling the fluke to complete its life-cycle. Since a much higher percentage of crawling Macoma specimens is infected than is the case with the stationary, usually deeply burrowed animals, it seems likely that the sporocysts form the stimulus which induces Macoma to crawl on the surface of the tidal flats.
IV. S U M M A R Y
At higher levels in the tidal zone conspicuous crawling-trails of Macoma balthica are sometimes found. The specimens making these trails turned out to be filled with sporocysts of an as yet unidentified Gymnophallid trematode. It was proved that the parasite does not develop any further in the mollusc, but that in a bird the sexually mature stage is reached within 24 hours. It is supposed that the parasite stimulates the host to crawling behaviour, thus increasing the chance of predation by a bird.
REFERENCES
BRAFIELD,A. E., 1963. The effects of oxygen deficiency on the behaviour of Macoma balthica (L.).--Anim. Behav. U (2-3): 345-346. BRAFIELD, A. E. & G. E. NEWZLL, 1961. The behaviour of Macoma balthica (L.).-J. Mar. biol. Ass. U.K. 44: 81-87. HAGMEmR, A. & R. KKNDLER, 1927. Neue Untersuchungen im nordfriesischen Wattenmeer und auf den fiskalischen Austerb~inken.--Wiss. Meeresunters., Helgoland 16: 1-90. HULSCHER, J. B., 1964. Scholeksters en larnellibranchiaten in de Waddenzee.-Levende Nat. 67: 80-85. MORa~NS~N, T., 1922. Biologiske Studier over Sandstrandsfaunaen, smrlig ved de danske Kyster.--Vidensk. Meddr dansk naturh. Foren. 74: 23-57. THAMDRUP, H. M., 1935. Beitr~ige zur Oekologie der Wattenfauna. Meddr Kommn Havunders., Fiskeri 10 (2): 1-125.
25