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“Squatter” behaviour in soft-shelled foraminifera
Marine Micropaleontology, 16 (1990) 149-153 Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands
149
Short Note
"Squatter" Behaviour in Soft-shelled Foraminifera LEON MOODLEY Netherlands Institute for Sea Research, P.O. Box 59, Den Burg, Texel (The Netherlands) (Received August 17, 1989; revised and accepted October 4, 1989)
Abstract Moodley, L., 1990. "Squatter" behaviour in soft-shelled foraminifera. Mar. Micropaleontol., 16: 149-153. During culture experiments of various calcareous foraminiferal species, an unidentified heteromorphic, monothalamous, soft-shelled foraminiferid, without any agglutinated matter was observed to feed and increase in size. When offered empty quinqueloculine tests, it rapidly crawled into one and appeared as a typical living Quinqueloculina specimen with extended pseudopodia. Apart from being another microhabitat of foraminifera, this would add to the problems associated with the use of protoplasmic stains in distinguishing living specimens of benthic foraminifera from dead, empty shells and emphasizes the need to exercise extreme caution in order to avoid misinterpretations of "living" assemblages, which have consequences for the paleoecological interpretation of fossil assemblages.
Introduction
Soft-shelled foraminifera differ from other foraminifera in that they have no solid covering but a proteinous or membranous test with or without loosely agglutinated material that allows a certain amount of flexibility. They are protozoans which belong either to the suborder Allogromiina or to the suborder Textulariina, superfamily Astrorhizacea, family Saccamminidae, according to the classification of Loeblich and Tappan (1988). Several reports have been made of finding empty foraminiferal tests occupied by soft-shelled foraminifera; however, no reports have been made of observing the actual intrusion. I present a series of photographs depicting the various steps of a soft-shelled foraminiferid entering an empty calcareous foraminiferal test. Several workers Rhumbler, 1894, 1911; Christiansen, 1958; Phleger, 1960; Hope and 0377-8398/90/$03.50
Murphy, 1969; Murray, 1973; Arnold, 1974; Thistle, 1979, Gooday, 1984) have reported the occurrence of metazoans in empty foraminiferal tests, mostly in large, unbranched arenaceous tests. These tests would provide convenient shelter and protection against predation. Calcareous and small arenaceous tests are only occasionally occupied by metazoans, for they are difficult to enter and offer limited living space (Gooday, 1984). Rhumbler (1894, 1911) and Nyholm (1953, 1956) reported the occurrence of soft-shelled foraminifera in empty tests of large arenaceous species. Rhumbler (1894, 1911 ) also suggested that certain species of softshelled foraminifera are restricted to this habitat. Gooday (1986a) found that soft-shelled forms made up 8.8-27.4% of the living foraminiferal assemblages from the Porcupine Seabight (southwest of Ireland, 1330 m depth) and that 2.2-12.2% of all soft-shelled foraminifera occupy empty globigerinacean (planktic) tests.
© 1990 Elsevier Science Publishers B.V.
150
L. MOODLEY
PLATE I Different shapes exhibited by a soft-shelled foraminiferid ( 1,2 ) and the actual intrusion ( 3-6 ) of an empty quinqueloculine test. All magnifications 100 × . 1. Elongate shape. 2. A more rounded shape. 3.45 minutes after being offered an empty test. 4. Eight minutes later. 5. Six minutes later. 6. Six minutes later, where the soft-shelled foraminiferid has totally moved into the empty test and now appears as a typical living Quinqueloculina specimen with extended pseudopodia.
151
"SQUATTER" BEHAVIOUR IN SOFT-SHELLED FORAMINIFERA
The invaded globigerinacean test would stain with rose Bengal, but the protoplasmic remnants of the original inhabitant is easily distinguished from the invading foraminiferid; the protoplasm of the invading foraminiferid is dense, more granular and are often associated with stercomata (oval masses of waste material within the cytoplasm ) as well as external structures such as cytoplasmic lumps and tubes (Gooday, 1986a).
Description To gain more insight into the vertical distribution (Corliss, 1985) of calcareous foraminifera in the sediment, several culture experiments are currently in progress. Sediment samples were obtained from the southern North Sea (40 m depth) using a modified Reineck box corer. This area is characterized by having a POC content of 1.29% and a median grain size of 83/tm. Subsamples were taken at different depth intervals in the sediment in order to have living specimens from different microhabitats. In the laboratory individual calcareous specimens were isolated and set in culture under the following conditions: 12 h light/12 h dark and maintained at an ambient temperature of 15 ° C. Filtered seawater was used as culture medium and detritus < 50 #m removed from the surface sediment was offered as food. Seawater is replaced once a week and food once every forthnight. During the routine observation of a calcareous species from the surface sediment (01 cm), 9 days after the initiation of the culture, an unidentified, heteromorphic, monothalamous soft-shelled foraminiferid devoid of agglutinated matter was discovered. Since the soft-shelled specimen was not isolated and set in culture it must have been in the detritus and was only observable when it reached a larger size. The soft-shelled foraminiferid was observed to feed and continuously take on different shapes varying from elongate to more rounded with long pseudopodia branching out (Plate I, 1,2). It remained unattached and de-
void of agglutinated material. The size of this specimen, after 10 days, was + 410 pm with pseudopodia reaching lengths of almost 13 times this size. When offered empty quinqueloculine tests it rapidly (within 1 hour) crawled into one and appeared as a typical living Quinqueloculina specimen (Plate I, 3-6). On the other hand, another unidentified softshelled specimen (removed from the 3-4 cm depth interval), that initially had quartz attached to its test, was first offered an empty quinqueloculine test, which it refused. When quartz grains were added to the culture, it actively collected a few grains around its membranous test, showing a distinct preference to quartz grains rather than empty shells. Thus, it appears that not all soft-shelled species inhabit empty foraminiferal tests and the type of test that can be occupied may depend upon the size and flexibility of the soft-shelled species.
Discussion It is clear that benthic foraminifera have distinct microhabitats. Corliss (1985) and Gooday (1986b) discussed respectively the microhabitats of calcareous and some soft-shelled foraminifera within deep-sea sediment. Empty foraminiferal tests form another microhabitat utilized by foraminifera. An advantage of this mode of life is the acquisition of a hard protective covering at low energy costs. It is important to distinguish living from dead individuals in ecological studies of benthic foraminifera with respect to applications in paleoecology, especially in shelf seas where dead assemblages differ significantly from the living (stained) assemblages ( Murray, 1976 ). The use of protoplasmic stains are generally favoured over the actual observation of cytoplasmic activity, which is very time consuming. Rose Bengal is a commonly used protoplasmic stain; however, since its original introduction (Walton, 1952) several limitations have been reported. Protoplasm of dead foraminifera may not decay for some months (Boltovskoy and
152
Lena, 1970) and could be included in the live counts leading to misinterpretations in cases where death is rapidly followed by transport to a depositional area (Le Calvez and Cesana, 1972). Empty tests occupied by organic material also stain with rose Bengal but its pink colour is easily distinguished from the intense red colour of stained protoplasm~ which is generally restricted to the initial chambers in living specimens (as observed in transparent living specimens in culture). Small soft-shelled foraminifera which inhabit the empty tests of small benthic foraminifera and have no external structures to distinguish them from the original inhabitant add to the problems inherent in the use of protoplasmic stains. The magnitude of this problem would depend on the number of species capable of this "squatter" behaviour and the quantity of suitable empty tests available. There is no direct solution to this problem, except that one would expect the invading soft-shelled foraminiferid to occupy the final chambers of an empty test and thereby being distinguishable from the original inhabitants that geaerally have their protoplasm restricted to the initial chambers. This emphasizes the need to exercise extreme caution when using protoplasmic stains as a method of recognizing living specimens. On the other hand, this "squatter" behaviour of certain soft-shelled foraminifera could be an explanation for the occurrence of stained species in areas where they are not expected. Apart from the advantage of soft-shelled foraminifera obtaining a hard protective cover at low energy costs, their existence together with their mode of life increase the diversity of this group of organisms. Acknowledgements I thank T.C.E. van Wee~ing and J.E. van Hinte for their fruitful suggestions during the preparation of this manuscript and G. Chmura for her corrections of the English text. Ch.
L. MOODLEY
Hemleben (Tiibingen) is acknowledged for his stimulation and interest. References Arnold, Z.M., 1974. Field and Laboratory techniques for the study of living Foraminifera. In: C.H. Hedley and C.G. Adams (Editors), Foraminifera. Acad. Press, London, Vol. 1, pp. 153-206. Boltovskoy, E. and Lena, A., 1970. On the decomposition of the protoplasm and the sinking velocity of the planktonic foraminifers. Int. Rev. Gesamten Hydrobiol., 55: 797-804. Christiansen, B., 1958. The foraminifer fauna in the Drobak Sound in the Oslo Fjord (Norway). Nytt. Mag. Zool., 6: 5-84. Corliss, B.H., 1985. Microhabitats of benthic foraminifera within deep-sea sediments. Nature, 314: 435-438. Cutler, E.B., 1973. Sipuncula of the western Atlantic. Bull. Am. Mus. Nat. Hist., 152: 103-204. Gooday, A., 1984. Records of deep-sea rhizopod tests inhabitated by metazoans in the North-east Atlantic. Sarsia, 69: 45-53. Gooday, A., 1986a. Meiofaunal foraminiferans from the bathyal Porcupine Seabight (north-east Atlantic ): size structure, standing stock, taxonomic composition, species diversity and vertical distribution in the sediment. Deep-Sea Res., 33 (10): 1345-1373. Gooday, A., 1986b. Soft-shelled foraminifera in meiofaunal samples from the bathyal northeast Atlantic. Sarsia, 71: 275-287. Hope, W.D. and Murphy, D.G., 1969. Syringonomous typicus new genus, new species (Enoplida: Leptosomatidae) a new marine nematode inhabiting arenaceous tubes. Proc. Biol. Soc. Wash., 82: 511-518. Le Calvez, Y. and Cesana, D., 1972. D~tection de l'~tat de vie chez les Foraminif'eres. Ann. Pal~ontol. (Invertebr.), 58(2): 129-134. Loeblich, A.R. and Tappan, H., 1988. Foraminiferal genera and their classification. Van Nostrand Reinhold Company, New York, N.Y. (2 vols. ). Murray, J.W., 1973. Distribution and ecology of living benthic foraminifera. Crane, Russak and Co., New York, N.Y., 274 pp. Murray, J.W., 1976. Comparative studies of living and dead benthic foraminiferal distributions. In: R.H. Hedley and C.G. Adams (Editors). Foraminifera. Academic Press, London, Vol. 2, pp. 45-109. Nyholm, K.-G., 1953. Studies on Recent Allogromiidae: 1. Micrometula hyalostriata n.gen., n.sp., from the Gullmar Fjord, Sweden. Contrib. Cushman Found. Foraminiferal Res., 3: 14-17. Nyholm, K.-G., 1956. On the life cycle and cytology of the foraminifera Nemogullmia longevariabilis. Zool. Bidr. Uppsala, 31: 483-495.
"SQUATTER"BEHAVIOURIN SOFT-SHELLEDFORAMINIFERA Phleger, F.B., 1960. Ecology and distribution of recent Foraminifera. Johns Hopkins Press, Baltimore, M.D. 297 pp. Rhumbler, L., 1894. Beitrage zur Kenntnis der Rhizopoden. II. Saccammina sphaerica M. Sars. Zweiter Teil. Z. Wiss. Zool., 57: 587-617. Rhumbler, L., 1911. Die Foraminiferen (Thalamophoren) der Plankton-Expedition. Ergeb. Plankton Exped., Humboldt-Stiftung, 3: 1-331.
153 Thistle, D., 1979. Harpacticoid dispersion and biogenic structures: implications for deep-sea diversity maintenance. In: R.J. Livingston (Editor), Ecological processes in coastal and marine systems, Plenum Press, New York, N.Y., pp. 217-231. Walton, W.R., 1952. Techniques for recognition of living Foraminifera. Cushman Found. Foraminiferal Res., Contrib., 3 (2): 56-60.
149
Short Note
"Squatter" Behaviour in Soft-shelled Foraminifera LEON MOODLEY Netherlands Institute for Sea Research, P.O. Box 59, Den Burg, Texel (The Netherlands) (Received August 17, 1989; revised and accepted October 4, 1989)
Abstract Moodley, L., 1990. "Squatter" behaviour in soft-shelled foraminifera. Mar. Micropaleontol., 16: 149-153. During culture experiments of various calcareous foraminiferal species, an unidentified heteromorphic, monothalamous, soft-shelled foraminiferid, without any agglutinated matter was observed to feed and increase in size. When offered empty quinqueloculine tests, it rapidly crawled into one and appeared as a typical living Quinqueloculina specimen with extended pseudopodia. Apart from being another microhabitat of foraminifera, this would add to the problems associated with the use of protoplasmic stains in distinguishing living specimens of benthic foraminifera from dead, empty shells and emphasizes the need to exercise extreme caution in order to avoid misinterpretations of "living" assemblages, which have consequences for the paleoecological interpretation of fossil assemblages.
Introduction
Soft-shelled foraminifera differ from other foraminifera in that they have no solid covering but a proteinous or membranous test with or without loosely agglutinated material that allows a certain amount of flexibility. They are protozoans which belong either to the suborder Allogromiina or to the suborder Textulariina, superfamily Astrorhizacea, family Saccamminidae, according to the classification of Loeblich and Tappan (1988). Several reports have been made of finding empty foraminiferal tests occupied by soft-shelled foraminifera; however, no reports have been made of observing the actual intrusion. I present a series of photographs depicting the various steps of a soft-shelled foraminiferid entering an empty calcareous foraminiferal test. Several workers Rhumbler, 1894, 1911; Christiansen, 1958; Phleger, 1960; Hope and 0377-8398/90/$03.50
Murphy, 1969; Murray, 1973; Arnold, 1974; Thistle, 1979, Gooday, 1984) have reported the occurrence of metazoans in empty foraminiferal tests, mostly in large, unbranched arenaceous tests. These tests would provide convenient shelter and protection against predation. Calcareous and small arenaceous tests are only occasionally occupied by metazoans, for they are difficult to enter and offer limited living space (Gooday, 1984). Rhumbler (1894, 1911) and Nyholm (1953, 1956) reported the occurrence of soft-shelled foraminifera in empty tests of large arenaceous species. Rhumbler (1894, 1911 ) also suggested that certain species of softshelled foraminifera are restricted to this habitat. Gooday (1986a) found that soft-shelled forms made up 8.8-27.4% of the living foraminiferal assemblages from the Porcupine Seabight (southwest of Ireland, 1330 m depth) and that 2.2-12.2% of all soft-shelled foraminifera occupy empty globigerinacean (planktic) tests.
© 1990 Elsevier Science Publishers B.V.
150
L. MOODLEY
PLATE I Different shapes exhibited by a soft-shelled foraminiferid ( 1,2 ) and the actual intrusion ( 3-6 ) of an empty quinqueloculine test. All magnifications 100 × . 1. Elongate shape. 2. A more rounded shape. 3.45 minutes after being offered an empty test. 4. Eight minutes later. 5. Six minutes later. 6. Six minutes later, where the soft-shelled foraminiferid has totally moved into the empty test and now appears as a typical living Quinqueloculina specimen with extended pseudopodia.
151
"SQUATTER" BEHAVIOUR IN SOFT-SHELLED FORAMINIFERA
The invaded globigerinacean test would stain with rose Bengal, but the protoplasmic remnants of the original inhabitant is easily distinguished from the invading foraminiferid; the protoplasm of the invading foraminiferid is dense, more granular and are often associated with stercomata (oval masses of waste material within the cytoplasm ) as well as external structures such as cytoplasmic lumps and tubes (Gooday, 1986a).
Description To gain more insight into the vertical distribution (Corliss, 1985) of calcareous foraminifera in the sediment, several culture experiments are currently in progress. Sediment samples were obtained from the southern North Sea (40 m depth) using a modified Reineck box corer. This area is characterized by having a POC content of 1.29% and a median grain size of 83/tm. Subsamples were taken at different depth intervals in the sediment in order to have living specimens from different microhabitats. In the laboratory individual calcareous specimens were isolated and set in culture under the following conditions: 12 h light/12 h dark and maintained at an ambient temperature of 15 ° C. Filtered seawater was used as culture medium and detritus < 50 #m removed from the surface sediment was offered as food. Seawater is replaced once a week and food once every forthnight. During the routine observation of a calcareous species from the surface sediment (01 cm), 9 days after the initiation of the culture, an unidentified, heteromorphic, monothalamous soft-shelled foraminiferid devoid of agglutinated matter was discovered. Since the soft-shelled specimen was not isolated and set in culture it must have been in the detritus and was only observable when it reached a larger size. The soft-shelled foraminiferid was observed to feed and continuously take on different shapes varying from elongate to more rounded with long pseudopodia branching out (Plate I, 1,2). It remained unattached and de-
void of agglutinated material. The size of this specimen, after 10 days, was + 410 pm with pseudopodia reaching lengths of almost 13 times this size. When offered empty quinqueloculine tests it rapidly (within 1 hour) crawled into one and appeared as a typical living Quinqueloculina specimen (Plate I, 3-6). On the other hand, another unidentified softshelled specimen (removed from the 3-4 cm depth interval), that initially had quartz attached to its test, was first offered an empty quinqueloculine test, which it refused. When quartz grains were added to the culture, it actively collected a few grains around its membranous test, showing a distinct preference to quartz grains rather than empty shells. Thus, it appears that not all soft-shelled species inhabit empty foraminiferal tests and the type of test that can be occupied may depend upon the size and flexibility of the soft-shelled species.
Discussion It is clear that benthic foraminifera have distinct microhabitats. Corliss (1985) and Gooday (1986b) discussed respectively the microhabitats of calcareous and some soft-shelled foraminifera within deep-sea sediment. Empty foraminiferal tests form another microhabitat utilized by foraminifera. An advantage of this mode of life is the acquisition of a hard protective covering at low energy costs. It is important to distinguish living from dead individuals in ecological studies of benthic foraminifera with respect to applications in paleoecology, especially in shelf seas where dead assemblages differ significantly from the living (stained) assemblages ( Murray, 1976 ). The use of protoplasmic stains are generally favoured over the actual observation of cytoplasmic activity, which is very time consuming. Rose Bengal is a commonly used protoplasmic stain; however, since its original introduction (Walton, 1952) several limitations have been reported. Protoplasm of dead foraminifera may not decay for some months (Boltovskoy and
152
Lena, 1970) and could be included in the live counts leading to misinterpretations in cases where death is rapidly followed by transport to a depositional area (Le Calvez and Cesana, 1972). Empty tests occupied by organic material also stain with rose Bengal but its pink colour is easily distinguished from the intense red colour of stained protoplasm~ which is generally restricted to the initial chambers in living specimens (as observed in transparent living specimens in culture). Small soft-shelled foraminifera which inhabit the empty tests of small benthic foraminifera and have no external structures to distinguish them from the original inhabitant add to the problems inherent in the use of protoplasmic stains. The magnitude of this problem would depend on the number of species capable of this "squatter" behaviour and the quantity of suitable empty tests available. There is no direct solution to this problem, except that one would expect the invading soft-shelled foraminiferid to occupy the final chambers of an empty test and thereby being distinguishable from the original inhabitants that geaerally have their protoplasm restricted to the initial chambers. This emphasizes the need to exercise extreme caution when using protoplasmic stains as a method of recognizing living specimens. On the other hand, this "squatter" behaviour of certain soft-shelled foraminifera could be an explanation for the occurrence of stained species in areas where they are not expected. Apart from the advantage of soft-shelled foraminifera obtaining a hard protective cover at low energy costs, their existence together with their mode of life increase the diversity of this group of organisms. Acknowledgements I thank T.C.E. van Wee~ing and J.E. van Hinte for their fruitful suggestions during the preparation of this manuscript and G. Chmura for her corrections of the English text. Ch.
L. MOODLEY
Hemleben (Tiibingen) is acknowledged for his stimulation and interest. References Arnold, Z.M., 1974. Field and Laboratory techniques for the study of living Foraminifera. In: C.H. Hedley and C.G. Adams (Editors), Foraminifera. Acad. Press, London, Vol. 1, pp. 153-206. Boltovskoy, E. and Lena, A., 1970. On the decomposition of the protoplasm and the sinking velocity of the planktonic foraminifers. Int. Rev. Gesamten Hydrobiol., 55: 797-804. Christiansen, B., 1958. The foraminifer fauna in the Drobak Sound in the Oslo Fjord (Norway). Nytt. Mag. Zool., 6: 5-84. Corliss, B.H., 1985. Microhabitats of benthic foraminifera within deep-sea sediments. Nature, 314: 435-438. Cutler, E.B., 1973. Sipuncula of the western Atlantic. Bull. Am. Mus. Nat. Hist., 152: 103-204. Gooday, A., 1984. Records of deep-sea rhizopod tests inhabitated by metazoans in the North-east Atlantic. Sarsia, 69: 45-53. Gooday, A., 1986a. Meiofaunal foraminiferans from the bathyal Porcupine Seabight (north-east Atlantic ): size structure, standing stock, taxonomic composition, species diversity and vertical distribution in the sediment. Deep-Sea Res., 33 (10): 1345-1373. Gooday, A., 1986b. Soft-shelled foraminifera in meiofaunal samples from the bathyal northeast Atlantic. Sarsia, 71: 275-287. Hope, W.D. and Murphy, D.G., 1969. Syringonomous typicus new genus, new species (Enoplida: Leptosomatidae) a new marine nematode inhabiting arenaceous tubes. Proc. Biol. Soc. Wash., 82: 511-518. Le Calvez, Y. and Cesana, D., 1972. D~tection de l'~tat de vie chez les Foraminif'eres. Ann. Pal~ontol. (Invertebr.), 58(2): 129-134. Loeblich, A.R. and Tappan, H., 1988. Foraminiferal genera and their classification. Van Nostrand Reinhold Company, New York, N.Y. (2 vols. ). Murray, J.W., 1973. Distribution and ecology of living benthic foraminifera. Crane, Russak and Co., New York, N.Y., 274 pp. Murray, J.W., 1976. Comparative studies of living and dead benthic foraminiferal distributions. In: R.H. Hedley and C.G. Adams (Editors). Foraminifera. Academic Press, London, Vol. 2, pp. 45-109. Nyholm, K.-G., 1953. Studies on Recent Allogromiidae: 1. Micrometula hyalostriata n.gen., n.sp., from the Gullmar Fjord, Sweden. Contrib. Cushman Found. Foraminiferal Res., 3: 14-17. Nyholm, K.-G., 1956. On the life cycle and cytology of the foraminifera Nemogullmia longevariabilis. Zool. Bidr. Uppsala, 31: 483-495.
"SQUATTER"BEHAVIOURIN SOFT-SHELLEDFORAMINIFERA Phleger, F.B., 1960. Ecology and distribution of recent Foraminifera. Johns Hopkins Press, Baltimore, M.D. 297 pp. Rhumbler, L., 1894. Beitrage zur Kenntnis der Rhizopoden. II. Saccammina sphaerica M. Sars. Zweiter Teil. Z. Wiss. Zool., 57: 587-617. Rhumbler, L., 1911. Die Foraminiferen (Thalamophoren) der Plankton-Expedition. Ergeb. Plankton Exped., Humboldt-Stiftung, 3: 1-331.
153 Thistle, D., 1979. Harpacticoid dispersion and biogenic structures: implications for deep-sea diversity maintenance. In: R.J. Livingston (Editor), Ecological processes in coastal and marine systems, Plenum Press, New York, N.Y., pp. 217-231. Walton, W.R., 1952. Techniques for recognition of living Foraminifera. Cushman Found. Foraminiferal Res., Contrib., 3 (2): 56-60.