EVIDENCE OF TEST DETACHMENT IN ASTRORHIZA LIMICOLA,
AND TWO CONSEQUENTIAL SYNONYMS: AMOEBA GIGANTEA AND
MEGAMOEBOMYXA ARGILLOBIA (FORAMINIFERIDA)
TOMAS CEDHAGEN
SARSIA
&
OLE SECHER TENDAL
CEDHAGEN TOMAS & OLE SECHER TENDAL 1989 11 15. Evidence of test detachment in
Astrorhiza limicola, and two consequential synonyms: Amoeba gigantea and Megamoebomyxa argillobia (Foraminiferida). - Sarsia 74:195-200. Bergen. ISSN 0036-4827.
Laboratory observations and experiments demonstrate that the naked rhizopods Amoeba
gigantea SANDAHL, 1857 and Megamoebomyxa argillo~ia NYHOLM, 1950, and the foraminifers Astrorhiza arenifera STSCHEDRlNA, 1946, A. sabulifera STSCHEDRINA, 1946 and A. arctlca STSCHEDRINA, 1958 are synonyms of Astrorhiza limicola SANDAHL, 1857. The authorship
of the family Astrorhizidae should be ascribed to SANDAHL (1857) instead of BRADY (1881)
as usually done. Large, agglutinating foraminifers that can live outside the test in this
condition represent a promising tool for biological and experimental work on foraminifers.
Tomas Cedhagen, Department of Zoology, Division of Morphology and Ecology, University of G6teborg, P. O. Box 25059, S-400 31 G6teborg, Sweden. - Ole Secher Tendal, Zoological Museum, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen
(b, Denmark.
INTRODUCTION
The large arenaceous foraminifer Astrorhiza limicola SANDAHL, 1857 is widely distributed in the
North Atlantic coldwater regions, where it occurs
mostly at depths between 15 and 50 m. Because the
species is conspicuous, common in many localities,
and shows some degree of variation (Fig. 1), a number of synonyms have been published (CUSHMAN
1918; BUCHANAN & HEDLEY 1960).
Previous studies with living A. limicola established that, under certain circumstances, specimens
can leave the test and build a new one (SCHULZ
1915), or can be squeezed out of the test and survive (BucHANAN & HEDLEY 1960). These phenomena
were observed during recent work on the feeding
biology of the species (CEDHAGEN 1988) which demonstrated that, in certain cases, some specimens
can survive as nude, free amoeboid forms. Such
amoebae have been seen by previous workers and,
since they were not considered to have any relationship with A. limicola, they were described as new
species and placed in other classes of the Rhizopodea. In this paper we synonymize two such naked,
amoeboid organisms, Amoeba gigantea SANDAHL,
1857 and Megamoebomyxa argillobia NYHOLM,
1950, with Astrorhiza limicola SANDAHL, 1857.
MATERIAL AND METHODS
Sediment was sampled with a detritus sledge at numerous
localities in Kosterfjorden on the Swedish west coast from
Yttre Vattenholmen to the harbour of Stromstad, at
20-40 m depth. Part of each sample (2~0 kg) was left
in a container for 2-14 days without changing the water.
The remaining material was sieved through a I-mm sieve,
and the Astrorhiza specimens were sorted out and kept
in aquaria with running seawater.
.
No specimens of A. gigantea could be found 10 the
Swedish Museum of Natural History, Stockholm. No type
specimens of Megamoebomyxa argillobia, were preserved
because of the fragility of this form (Prof. Nyholm, pers.
commn).
RESULTS
When sediment samples with buried A. limicola
were left, amoeboid organisms large enough to be
seen easily with the naked eye appeared on the
sediment surface after a few days.
.
The organisms were opaque white in colour. The
body form varied from irregulary star-shaped to
rounded with a lobed outline (Fig. 2). Maximum
diameter including the pseudopodia varied according to shape and was between 1 and 10 cm. At first
glance the pseudopodia looked like coarse filopodia, but when examined microscopically, they
proved to be granulo-reticulopodia.
The organisms moved a distance of up to a few
cm per day, sometimes even climbing up the container walls. As long as they were left in the container with sediment they made no attempt to construct an agglutinated test. However, when transferred to a dish with fresh seawater and given loose
materials, they invariably built a test in a very short
time, often within a day. They did not seem to be
selective and used any available particles, including
clay and sand from the original sediment, residues
from a plankton sample, and fragmented spinach,
which was supplied as food. In all cases, the organisms with their tests were typical A. limicola.
195
B
A
K
s
y
u
T
z
AA
w
v
AB
AC
AD
x
AE
Fig. 1. Specimens of Astrorhiza limicola SANDAHL, collected in Kosterfjorden, Swedish west coast, c. 40 m, showing
the variation in test morphology. Specimens A, B, and C have incorporated grains almost as large as the test. The
specimens are arranged according to decreasing grain size. Scale bar, 2 mm.
196
Fig. 2. Specimen of Astrorhiza limicola SANDAHL, collected in Kosterfjorden, Swedish
west coast, c. 40 m, caused to leave its test due to anoxic conditions. Scale bar, 1 mm.
Nude, amoeboid. organisms were also obtained
by removing the test from Astrorhiza limicola specimens under a stereo-microscope. The white sarcode
was very sticky and adhered to the forceps. Organisms treated in this way were in every detail identical to those appearing on the surface of the origi-
nal sample. Given particulate material, each specimen made a new test, typical for A. limicola.
Whatever their origin, the nude organisms survived for months and thrived on a diet of plankton
algae, as do normal A. limicola from the Swedish
west coast.
197
In a laboratory experiment three groups of 15,
30, and 200 specimens of A. limicola were placed'
in closed glass containers of identical size, and with
the same quantity of seawater at 15° C. After three
days, all specimens in the group of 200 left their
tests, while members of the two other groups behaved as usual. The three containers were then transferred to a 4° C room and left for 2 l;2 months. The
two small groups continued as before, while after
some time many of the naked A. limicola specimens were seen climbing up the glass sides, probably because of oxygen deficiency. Small amounts of
hydrogen sulphide (H2S) developed in detrital residues on the bottom. No traces of hydrogen sulphide
could be observed in the containers with the two
small groups.
DISCUSSION
NYHOLM (1950), when describing M. argillobia,
briefly mentioned the possibility of a connection
between Megamoebomyxa and Astrorhiza when
saying (p. 96): '
Astrorhizid, when deprived of
its mud covering,
or ... represent some stage in
an Astrorhizid Life cycle?', but answered his own
question with: 'The results of culturing and observations in the habitat do not, however, bear out such
an assumption.' He was the first to observe that the
naked sarcode can live for some months in the laboratory. NYHOLM referred to neither SANDAHL nor
SCHULZ.
Megamoebomyxa has been difficult to place systematically. After a rather lengthy discussion, NyHOLM (1950) gave it a provisional place in the Vampyrellidae (Order Proteomyxida), as did also KUDO
(1966). BovEE (1985) placed it in incertae sedis position within the class Acarpomyxea.
The history
Astrorhiza limicola, Amoeba gigantea, and Megamoebomyxa argillobia were all described from the
same local area of the Swedish west coast, a muddy
bottom (40-70 m depth) in Gullmarsfjorden, near
Kristineberg Marine Biological Station. In the collections at the Swedish Museum of Natural History,
Stockholm, there are three specimens of A. limicola collected at the same locality by Loven in the
mid-1800's.
SANDAHL (1857) gave short diagnoses in Latin and
more lengthy and detailed descriptions in Swedish
of Astrorhiza limicola and Amoeba gigantea. He
found numerous specimens of whitish Amoeba gigantea one summer morning in 1856 on the surface
of a clay sample that had been standing overnight
(THEEL 1930). Such details as network and two-way
streaming of the pseudopodia are mentioned in his
description, but although to some degree he compared the specimens with Astrorhiza limicola, he
does not seem to have thought of any connection
between them, probably because, despite careful
search of the clay sample, he found only one specimen of A. limicola.
We have found no further mention of A. gigantea.
except by RHUMBLER (1904: 201) who transferred
the species to his genus Dactylosaccus (Foraminifera).
SCHULZ (1915) was the first to note that Astrorhiza limicola can leave its test, and he gave detailed accounts of the appearance and behavior of
naked specimens. Probably, he did not know about
Sandahl's description of Amoeba gigantea. However, SCHULZ (1915) figures alone give a strong impression of similarity between naked Astrorhiza limicola and Amoeba gigantea.
A. limicola in the naked condition
SCHULZ (1915) believed that A. limicola left its test
because of a rise in temperature in the aquarium.
Our aquarium observations indicate that to leave
the test is not a regular occurring phenomenon.
At the localities, where A. limicola lives, the temperature never rises drastically, but there is a strong
seasonal sedimentation of phytoplankton blooms
which may lead occasionally to oxygen deficiency;
in such conditions the large surface of the free sarcode may aid respiration. Changing current conditions may sometimes stir up the uppermost sediment layer, burying Astrorhiza under as much as
1 cm of sediment. The sarcode of a buried specimen
might survive by climbing to the surface and building a new test.
Following a thorough histological study, SCHULZ
(1915) concluded that leaving the test has no connection with sexual reproduction in Astrorhiza limicola, at least under the conditions prevailing in the
aquarium. However, we envision three reproductive
roles that the naked stage could fulfil. 1) Asexual
division into two or more individuals might be followed by each offspring leaving the old test and
building a new one. BEssELs (1875:274) reported
observing something similar although, because of
the conditions under which the observations were
made, we doubt his interpretation. 2) Because we
do not find A. limicola specimens smaller than
1.5 mm in size, it is possible that young individuals
live naked, well below the sediment surface. 3) The
reproductive cycle of A. limicola is not known, and
hence naked individuals may represent one generation which occurs only rarely, like, for example, the
rare agamonts of Saccammina alba HEDLEY, 1962,
198
which are found only during a short period of the
year (GOLDSTEIN 1988).
BUCHANAN & HEDLEY (1960) reported that A. limicola can be squeezed out of the test and survive.
The observation is confirmed here, and we found
no difference between specimens which were induced to leave their tests by themselves, and those
dissected out. BOWSER & DELACA (1985) reported
that the protoplasm of Astrammina rara RHuMBLER,
1931 also can be dissected out and be kept alive for
over two years. The ability to live without the test
may be widely found in larger, agglutinating foraminifers, and although its role under natural conditions should be better understood, it provides a
promising tool for biological and experimental work
on these organisms in the laboratory. The phenomenon has also been found in Jridia diaphana HERONALLEN & EARLAND, 1914 by CUSHMAN (1920) and
MARSZALEK & al. (1969) as well as in the marine
testacean 'Pontifex maximus' (PAGE 1983).
Taxonomical implications
Although their descriptions are separated by a century, Amoeba gigantea SANDAHL (see THEEL
1907:54) and Megamoebomyxa argillobia NYHOLM
were taken in the same local area, and appeared
under similar circumstances. In all details, except
for the maximum size and the occurrence, according
to NYHOLM (1950), of filopodia in Megamoebomyxa,
they are alike. On this basis, and supported by our
own observations, we conclude that they represent
naked specimens of Astrorhiza limicola. Amoeba
gigantea and M. argillobia are therefore synonyms
of A. limicola.
Based on test composition, STSCHEDRINA de scribed Astrorhiza limicola var. arenifera, A. limicola
var. sabulifera (1946:140), and A. limicola var. arctica (1958:120). The same author later regarded the
first two varieties as full species (STSCHEDRINA
1958:120, 1964:80), and formally gave species rank
to the latter (STSCHEDRINA 1964:91). BUCHANAN &
HEDLEY (1960:553) reported that A. limicola with
damaged test made repairs with any material offered. They also emphasized that, with the exception of the coarsest and finest fractions, all sediment size categories are indiscriminately used at the
given biotope. Referring to details of test construction, BUCHANAN & HEDLEY (1960:554) expressed
doubt about the distinct status of A. limicola var.
arenifera. SCHULZ (1915:217) pointed out that the
original and the regenerated tests of an individual
are often very dissimilar. Based on the reports by
BUCHANAN & HEDLEY and SCHULZ, and our own
observations, we consider A. arenifera, A. sabulifera, and A. arctica to be variants of the same speci-
es in which different materials are used to construct
the test. The names of these taxa are therefore synonyms of A. limicola (Fig. 1).
The taxonomical status of Astrorhiza limicola
Astrorhiza limicola is the type species of the genus
by monotypy. As first revisers, we give priority to
A. limicola over A. gigantea. Our reasons are.
1) The historically long and consistent usage of the
name A. limicola for a well-known and widely recognized species. 2) The name gigantea was used
for the sarcode only, and not the test which is the
decisive morphological expression of a foraminiferal
species for taxonomic identification.
The erection of the family Astrorhizidae is generally attributed to BRADY (1881:41). BRADY and all
the following authors unfortunately were not aware
that SANDAHL (1857:303) expressly erected the family when he wrote (translated from Swedish): ' .. .introduce Astrorhiza as the type for a fourth family,
which, in accordance with the remaining families,
should be named Astrorhizida.' Fortunately the same type genus and family definition are given by
SA.NDAHL and BRADY.
Variations in the behaviour of different populations
of A. limicola
CEDHAGEN (1988) pointed out that specimens from
the Swedish west coast invariably behave differently
than specimens from southern England, as described by BUCHANAN & HEDLEY (1960). In both cases
the observations were made in the laboratory.
Swedish west coast specimens adopt an upright
position, are sessile, and are suspension feeders
(occasionally deposit feeders). Specimens from
southern England lie flat, move around, and are
carnivorous. The only other observation of A. limicola behaviour that we are aware of, is by BESSELS
(1875:270). He saw, under inadequate laboratory
conditions, one specimen climb up a glass wall and
take a position at a right angle to the wall; this
might be considered the same as taking an upright
position.
Further insight into the population differences
can probably be gained through caryological and
electrophoretical investigations.
ACKNOWLEDGEMENTS
The authors are very much indebted to Dr L. Afzelius,
Director of Tjiirn6 Marine Biological Laboratory, Str6mstad, Sweden for providing excellent working conditions.
We thank Drs R. OlerOd and A. Waren for their assistance during our visit to The Swedish Museum of Natural
History, Stockholm and Professor K.-G. Nyholm, G6teborg, for giving us valuable information. We also thank
Dr A. Gooday for reviewing the manuscript.
199
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