Laguna (2021) 28: 15-35

ISSN 2185-2995

Review
Turbellarian egg capsule as one type of aquatic palynomorph;reconsideration of Tintinnomorph
Kazumi Matsuoka1,2* and Takuto Ando3
Abstract: Tintinnomorphs have attracted attention in the analysis of aquatic palynomorphs dueto their characteristic funnel, bell, pitcher, or cup-shaped morphology, although they have notbeen predominant in aquatic palynomorph assemblages in comparison with dinoflagellate cysts,
microforaminiferal linings and crustacean resting eggs. In this paper, through an examination of

the history of tintinnomorph research, the origin of tintinnomorphs becomes clearer. Recent studies
of aquatic or non-pollen palynomorphs have revealed that the tintinnomorphs consist of various

remains from several types of organisms of different origins, including ciliate lorica, resting cysts,
and turbellarian egg capsules. Considering these results, several technical terms for descriptionof turbellarian egg capsules are reassessed. Also, new insight on the origin of acritarchs called
Palaeostomocystis and Beringiella is shown based on comparison of morphological features ofmodern turbellarian egg capsules. However, the establishment of a species concept for turbellarianegg capsules and their usefulness as paleo-environmental indicators will require further
investigation of modern turbellarian egg capsules.

Key words: tintinnomorph, turbellaria, palynomorph, egg capsule, Palaeostomocystis, Beringiellacysts are attracting attention as powerful indicators

Introduction

for paleoclimatological and paleoenvironmental

Holocene to Late Pleistocene sediments contain various

reconstruction, and basic research on their morphology,

microfossils (remains). In the field of micropaleontology,

chemical composition of their walls, physiology andmicrofossils (remains) composed of organic walls have

ecology is actively progressing (e.g. Van Nieuwenhove

et al., 2020 for dinoflagellate cysts). On the other hand,been collectively called palynomorphs (Travers, 2007).
Among them, pollen, fern spores, and dinoflagellate

palynomorphs (e.g., ciliate cysts, foraminiferal linings,

1

Institute for East China Sea Research, Nagasaki University; Taira-machi 1551-7, Nagasaki 850-2213, Japan.

2

Osaka Museum of Natural History; Nagai Park 1-23, Sumiyoshi-ku, Osaka 546-0034, Japan.

3

Estuary Research Center (EsReC), Shimane University; Nishikawatsu-cho 1060, Matsue 690-0823, Shimane, Japan.

* Corresponding Author

Note : In this article, many published studies are introduced and followed together with photo figures and drawings. When we refer these figures in the text,
abbreviations with small letters are used like pl. and fig.
受付日：2021 年 6 月 27 日，受理日：2021 年 10 月 19 日，WEB 掲載日：2021 年 12 月 4 日

15Kazumi Matsuoka・Takuto Ando

resting eggs and body fragments of cladocerans, anda nd Cestoda. However, as a result of molecula r

components in comparison with major pollen, fern

is a paraphyletic group. Therefore, it is not maintained as

coenobia of green algae) have been regarded as minor

phylogenetic studies, it has become clear that Turbellaria

spores, and dinoflagellate cysts. If they are dominant,a class and has been dismantled. According to Ruggierothese palynomorphs have been especially noticed. In

et al. (2015), the Platyhelminthes are classified into

recent years, interest has been focused on palynomorphs

two subphyla and four classes. Turbellaria has beenother than pollen, fern spores, and dinoflagellate cysts,

subdivided into subphylum Catenulidea, class Catenuida

and research results, including reviews, have been(e.g., Stenostomum saliensa, Catenula lemnae) andpublished one after another (Hartman et al., 2018;subphylum Rhabditophora (class MacrostomorphaMatsuoka and Ishii, 2018; Pieńkowski et al., 2020; Mudie( Polycladidea, e.g., Pseudoceros bimarginatus ，et al. 2021; McCarthy et al., 2021).

Pseudoceros scintillates), class Polycladidea (e.g.,

On the other hand, these minor palynomorphs are often

Notoplana humilis), a nd class Neoophora (e.g.,

the remains of dormant cells and have not received much

Coniochaeta hoffmannii). Although Monogenea (e.g.,

attention from modern biologists. Micropaleontologists

Hexostoma thynni), Trematoda (e.g., Paradeontacylix

have basically endeavored to construct a classification

grandispinus), and Cestoda (e.g., Taenia saginata) havesystem based on the microfossil morphology. However,been confirmed to be cohesive as taxa, they are now

at ti mes, t hese resea rches a re a too focused on

positioned as infraclasses within class Neoophora. Sincemorphological information (e.g. van Waveren, 1993),

most of the taxa producing egg capsules, such as theand lose sight of the affinity of the remains. One suchfamilies Umagillidae, Dalyelliidae and Typhloplanidae,

example is the study of hystrichospheres related to fossil

were formerly classified into the Turbellaria, it may bedinoflagellates (Sarjeant, 1974). Since the dormant cells

preferential to keep the term “Turbellaria”, which is(cysts) remaining in the sediment and their motile cells

not used as a formal taxonomic name anymore. In this(plankton) are morphologically different, a germination

article, we propose to use “turbellaria” and focus only on

experiment was required to establish a correspondence

the reconsideration of tintinnomorphs, some of which are

between both. Such new methods were needed forconsidered to be produced by turbellarians (Table 1).

further research developments. Thus, increasing the basic

biological information about organic microfossils in

1-2. Turbellarian egg capsules in plankton samples

studies will be useful for future paleoenvironmental anddifferent organisms as "Geschwänzte Cyste" in the

Recent studies (e.g., Haas, 1994; Hartman et al., 2018;

fig. 5) at Karajak Fjord on the west coast of Greenland;

sediments that were not fully characterized in previous

Lohmann (1910) introduced two morphologically

paleoclimate researches.

plankton collected by Vanhöffen (1897, p. 287, taf. 6,

Mudie et al., 2021) have pointed out that fossils called

Lohmann (1910) explained that they are the same twotintinnomorphs by van Waveren (1993), which weretypes described by Kräfft (1906) as follows (Translatedgrouped as palynomorphs with similar morphology, havefrom the German description; Fig. 1):

different biological affinities. Turbellarian egg capsules“1. Spindle-shaped egg forma a (Kräfft 1906, fig. 7a, b =are the origin of one of the main types of tintinnomorphs.

Lohmann 1910, fig. 15 a, b) (reproduced in Fig. 1A).

Therefore, in this study, we will review moder n

as "The bluish green to brownish shell is slender andturbellarian egg capsules collected in sediments andspindle-shaped and ends on both sides in a thin thread

propose future research directions from the viewpoint ofof the same color about 1/3 of the length of the whole

palynology.

organism, one of which occasionally shows an adhesive

disc-shaped thickening, which makes the eggs likely tostick. Especially since only empty casings were found

1. Modern Platyhelminthes

floating freely, which were either still provided with

1-1 Taxonomy of Turbellaria (flatworms)

both end threads, had split open at the side (fig. 7a) or

Traditionally, the phylum Platyhelminthes was divided

in which a small cover with a cut surface inclined to theinto four classes: Turbellaria, Monogenea, Trematoda,

longitudinal axis had jumped off (fig. 7b). In the large
16

17

Rhabdocoela; Umagillidae
Rhabdocoela; Umagillidae
Rhabdocoela; Umagillidae
Rhabdocoela; Umagillidae
Rhabdocoela; Umagillidae
Rhabdocoela; Umagillidae
Rhabdocoela; Umagillidae
Rhabdocoela; Dalyelliidae
Rhabdocoela; Dalyelliidae
Rhabdocoela; Typhloplanidae
Rhabdocoela; Typhloplanidae
Rhabdocoela; Dalyelliidae
Neorhabdocoela
Rhabdocoela; Urastomidae
Rhabdocoela; Polycystididae
Rhabdocoela; Umagillidae
Rhabdocoela, Microstomidae
Rhabdocoela; Plagiostomidae
Rhabdocoela; Dugrsiidae
Rhabdocoela; Stenostomidae
Rhabdocoela; Dalyelliidae
Rhabdocoela; Dalyelliidae
Rhabdocoela; Dalyelliidae
Rhabdocoela; Dalyelliidae
Rhabdocoela; Typhloplanidae
Rhabdocoela; Typhloplanidae
Rhabdocoela; Typhloplanidae
Rhabdocoela; Typhloplanidae
Rhabdocoela; Typhloplanidae
Rhabdocoela; Typhloplanidae
Rhabdocoela; Gyratricidae
Rhabdocoela; Polycystididae
Rhabdocoela; Dalyelliidae
Rhabdocoela; Dalyelliidae
Rhabdocoela; Dalyelliidae

Anoplodium hymanae Shinn, 1983

Wahlia pulchella Kozioff and Shinn, 1987
Syndesmis dendrastorum Stunkard and Corliss, 1951
Syndesmis collongistyla (Hertel, Dlszynski and Ubelaker, 1990) Jondelius, 1996
Syndesmis rubida Kozioff and Westervelt, 1990
Syndesmis albida Kozioff and Westervelt, 1990
Syndesmis evelinae (Marcus, 1968) Hertel and Duszynski, 1991
Microdalyellia armigera (Schmidt, 1862) Gieysztor, 1938
Gieysztoria virgulifera (Plotnikow, 1906) Ruebush and Hayes, 1939
Strongylostoma radiatum (Müller OF, 1773) Ørsted, 1844
Mesostoma lingua (Abildaard, 1789) O. Schmidt, 1848
Gyratrix hermaphroditus Ehrenberg, 1831
Neorhabdocoela unknown

Urastoma cyprinae (Graff, 1882) Westblad, 1955

Gyratrix hermaphroditus Ehrenberg, 1831
Syndesmis patagonica Brogger and Ivanov, 2010
Microstomum lineare (O. F. Muller, 1773) Örsted, 1843
Plagiostomum lemani Forel and Du Plessis, 1874
Dugesia gonocephala Duges, 1850
Stenostomum sp.
Microdalyellia sp.
Dalyellia sp.
Gieysztoria sp.
Typhloplana viridata (Abldgaard, 1789) Ørsted, 1843
Strongylostoma radiatum (O.F. Muller, 1773) Ørsted, 1844
Rhynchomesostoma rostratum (O.F. Muller, 1773) Ørsted, 1844
Olisthanella truncula (O. Schmidt, 1858) Voigt, 1892
Mesostoma productum (O. Schmidt, 1848) O. Schmidt, 1858
Mesostoma lingua (Abildaard, 1789) O. Schmidt, 1848
Bothromesostoma personatum (O. Schmidt, 1848) Braun, 1885
Gyratrix hermaphroditus Ehrenberg, 1831
Opisthocystis (Polycystis) goettei Bresslau, 1906
Gieysztoria garudae Van Steenkiste, Van Mulken and Artois, 2012
Gieysztoria ashokae Van Steenkiste, Van Mulken and Artois, 2012
Gieysztoria stokesi Van Steenkiste, Van Mulken and Artois, 2012

Rhabdocoela; Umagillidae
Rhabdocoela; Dalyelliidae
Rhabdocoela; Dugeslidae
Rhabdocoela, Koinocystididae
Rhabdocoela, Koinocystididae
Rhabdocoela, Koinocystididae
Rhabdocoela, Koinocystididae

Syndesmis kurakaikina Monnens, Vanhove and Artois, 2019

Gieysztoria sp.
Girardia dorotocephala (Woodworth, 1987) Ball, 1974
Itaipusa novacaledonica Diez, Schockaert, Reygel and Artois, 2021
Reinhardorhynchus pacificus Diez, Schockaert, Reygel and Artois, 2021
Galapagetula cubensis Diez, Schockaert, Reygel and Artois, 2021
Simplexcystis asymmetrica Diez, Schockaert, Reygel and Artois, 2021

Classification followed by Turbellarian
WoRMS (World Register of Marine Species)
http://www.marinespecies.org/turbellarians/index.php
andINPN (Inventaire National du Patrimoine Naturel
https://inpn.mnhn.fr/espece/cd_nom/543104/tab/taxo?lg=en

Rhabdocoela; Umagillidae
Rhabdocoela; Umagillidae
Rhabdocoela; Umagillidae

Syndesmis aeethopharynx Westervelt & Kozloff, 1990
Syndesmis aonikenki Brusa, Montes, Marcotegui and Martorelli, 2017
Syndesmis selknami Brusa, Montes, Marcotegui and Martorelli, 2017

Temnocephala colombiensis Garcés, Puerta, Tabares, Lenis and Velàsquez, 2013 Rhabdocoela, Temnocephalidae

Rhabdocoela; Umagillidae
Rhabdocoela; Umagillidae
Rhabdocoela; Umagillidae

Order; Family
Rhabdocoela; Umagillidae
Rhabdocoela; Dalyelliidae
Rhabdocoela; Dalyelliidae

Ozametra arbora (Ozaki, 1932) Marcus, 1949
Provortex balticus (Schultze, 1851) Graff, 1882
Castrella pinguis (Silliman, 1884) Fuhrmann, 1884
Anoplodium parasita Schneider, 1858
Anoplodium stichopi Bock, 1925
Syndesmis echinorum Meixner, 1923
Syndesmis franciscana (Lehman, 1946) Marcus, 1949

SpeciesMorphology (Shape of egg capsule)

Roundly fusiform with hollow stalk, capsules smooth or decorated by small verrucae; capsules longer than about 160 µm,at the anterior end an opercular suture
Oval to diamond-shaped, posterior end with a short stalk that bears long fimaments
Ovoidal to shortly ellepsoidal with long stalk
ovoidal to subspherical with long filamentus stalk, 68-160 µm x 56-120 µm
elongate with long filamentus stalkelongate with long filamentus stalk
ovoidal with long filamentus stalk
ellipsoidal or ovoidal; width range: 70-120 µm, length range: 100-210 µm, wide pyrome: with fine operculum suture
truncated pyramid, wide pylome
spherical, wide pylome
sperical, radial operculum suture
Roundly cup-shaped (1-A, B) and cup-shaped (1-C, D) with stalk furnishing attachment apparatus, wide pylome
spherical with short stalk
oval or suboval cocoons which are thin-walled and contain several subspherical ovoidal egg capsules. Each egg capsulehas sealing zone in the shell. 219( 150-290) x 170 (100-260) mm
ovoidal to ellepsoidal, yellowish brown, large pylome
ovoidal with very long filamentus stalk
Yellowish, spherical (200-250 mm)
Dark yellowish, ovoidal with stalk
black to brownish orange, spherical (2000 mm)
egg capsulesingle egg capsule, no stalkmany egg capsules in animal tissue, no stalk
single egg capsule, no filament
ovoidal with operculum suture
yellowish orange to reddish brown, sperical with operculum suture, 144 ~ 330 µm
spherical, reddish brown, no stalk, 155-185mm
spherical to ellpsoidal, yellowish brown, no stalk, 200 mm
Elongatedly ovoidal, 160 mm
egg; ovoidal, yellowish to reddish brown, 270-360 mm
egg; spherical, brwon
usually one and rarely two-to three egg capsules involving one or rarly two eggs
subspherical, yelloish orange, short stalk, 350 mm
ovoidal to ellepsoidal (165x120mm)
egg-shell with sinuate outline
ovoidal to rhomboidal (180mm)
elongate egg capsule with shour stout stalk bearing basal attachment, large pylome bearing irregular suture of
operculum
yellowish brown, subspherical with very long filamentus stalkbrownish, ovoidal with long filamentus stalkbrownish, ovoidal with long filamentus stalk
ovoidal with long filamentus stalk (125 µm long and 85 µm wide), wide pylome with operculum bearing irregularsutureovoidal, brownish
Large spherical egg capsule with filamentus stalk, 2000 mm
not clearnot clearnot clearnot clear

ovoidal with slender stalkelongatedly ovoidal with short stalk
subspherical with filament

egg capsules collected from sediment; however, most of them do not mention species names.

Table 1 List of turbellarian species that produce egg capsules. There are many publications dealing with turbellarian

Turbellarian egg capsule as one type of aquatic palynomorph; reconsideration of Tintinnomorph

18

M: marine
B: brackish
F: freshwater

M
FW
M
F
F
F
F
F
F
F
F
F
F
F
F
F
F
M, B, FF
FW
FW
FW
FW (ectosymbiont)
M (endosymbiont)
M (endosymbiont)
M (endosymbiont)
M (endosymbiont)
FW (free living)F
M (free living)M (free living)M (free living)M (free living)

habitatM (endosymbiont)MM
M (endosymbiont)
M (endosymbiont)
M (endosymbiont)
M (endosymbiont)
M (endosymbiont)
M (endosymbiont)
M (endosymbiont)
M (endosymbiont)
M (endosymbiont)
M (endosymbiont)
M (endosymbiont)
FW (free living)
FW (free living)
FW (free living)
FW (free living)
FW (free living)as egg
as egg
as egguterus & alone
in uterus
as egg
as egguterus & alone
uterus?
as egg capsulein uterus

as egg

as egg capsuleas egg capsulesediment
in uterus
as egguterus & alone
uterusuterusin uterus
in uterus
in uterus
in uterus
sediment
sediment
sediment
sediment
sedimentmaterial
in uterus
as egg
as eggTable 1 Continued.

Diez et al. 2021

SU: sea urchin
SC: sea cucumber

only uterus shown (possibly not produce egg capsule)endosymbiont of sea urchin
endosymbiont of sea urchin
endosymbiont of sea urchin

Brusa et al. 2017

description only

description only
description only
description only
description only, M. armigera, M fusca, M. fairchildi, M brevispina, M. turugae
description only
description only
description only
description only; sometimes as plankton
description only
description only
description only; as plankton
description only
description only

endosymbiont of mussels
followed Haas (1996)
endosymbiont of sea urchin

Two types; 1 A-B (different Surface ornaments)
Some other Mesostoma species included
Four Ecotypes; 1-A, 1-B, 1-C, 1-D (different Surface ornaments)

host Pomacea sp. (freshwater snail)

Monnens et al. 2019
Yamazaki 2020
Kawakatsu et al. 2020

Remarks

as Castrella truncata Kepner & Gilbert, 1931
host; sea cucumber
host; sea cucumber
host; sea cucumber
host; sea cucumber
host; sea cucumber. Newly produced capsules contain a single zygote (rarely 2-3 zygotes)
the host; Stichopus californicus (SC)endosymbiont of Dendrastar excentricus (SC)endosymbiont of sea urchin
endosymbiont of sea urchin
endosymbiont of sea urchin
endosymbiont of sea urchin
Five types; 1 A-E (different Surface ornaments)

endosymbiont of sea cucumber

Garcés et al. 2013
Monnens et al. 2017

van Steenkiste et al. 2012

Okugawa K. in Ueno M. 2010

González et al. 2005
Gelorini et al. 2011
Brogger and Ivanov 2010

Hass 1996

Hertel and Duszynski 1991

Kozioff and Westervelt 1990

Shinn 1986, Kozioff and Shinn 1987
Shinn 1988
Hertel et al. 1990

Shinn 1985

Uchida et al. 1965

Reference

Kazumi Matsuoka・Takuto Ando

Turbellarian egg capsule as one type of aquatic palynomorph; reconsideration of Tintinnomorph

Fig. 1 Turbellarian egg capsules in plankton sample collected by Vanhöffen (1897)
as cysts possessing a tail (A from fig. 15 and B from fig. 16 in Lohmann, 1910).

"spindle egg" there is no indication of the seam along

Resource Conservation Association, 2015). These

thickness 60 μm. Probably Kräfft rightly considered thesecapsules. Therefore, these spindle forms may be identicalwhich the lid comes off. The length was about 1 mm, themorphologies are different from typical turbellarian egg

as trematode eggs and they were found in the plankton of

to Neorhabdoceles (turbellaria) not Trematoda.

the North Sea off the Elbe and Weser estuaries.”

2. Study history of turbellarian egg capsules“2. Spindle-shaped egg forma b (Kräfft 1906, fig. 7c, d =as fossils preserved in sediments

Lohmann 1910, fig. 16a, b) (Fig. 1B).

as “Like the previous shape, but more rounded and witha seam running in an oblique direction; Adhesive threads

2-1 Freshwater sediments

drawing). Length 200–300 μm, thickness 100–170 μm”.

palynomorphs have occasionally been observed during

to be a pre-hatching egg capsule with filaments on both

sediments due to their high durability, but have beenwith a clearly defined adhesive disc (not shown on the

Brownish funnel-, bell-, pitcher-, and cup-shaped

It is inferred that the Spindle forma a of fig. 7a seems

pollen analysis studies carried out mainly in Holocene
recorded as "problematica" due to their unknown identity

sides, fig. 7b seems to be a post-hatching egg capsulelosing an operculum, and Fig. 7c, d are post-hatching egg(e. g., Erdtman, 1922; Nilsson, 1952). Many of them were

capsules with different morphologies.

records from freshwater sediments, but did not receive

Although Kräfft (1906) suggested these were eggs ofmuch attention because they were low in concentrationcompared to pollen, fern and fungal spores (e.g., Faegri

trematoda, they seem to be classified as the Rhabdocoela(turbellaria) rather than Trematoda, because theseand Iversen, 1989).

organisms illustrated have greenish to brownish wall of

H a r m s w o r t h (19 6 8) f o u n d t h e p r e s e n c e o f

egg capsules possessing a stalk as explained later. Some

Neorhabdoceles (Platyhelminthes) egg capsules inshaped eggs and Monogenean Vallisiopsis contorta has

and suggested them to belong to two types: a Gyratrix

Trmatoda species like Cardicola orientalis has crescent-sediment cores collected at Blelham Tarn, England,

fusiform eggs with long filaments at both ends and a non-

type: a dark-colored and wine glass-shaped body with or

pigmented and nearly transparent wall (Japan Fisheries

without striation and bearing stalk, and a Microdalyellia
19

Kazumi Matsuoka・Takuto Ando

type: dark-colored, U-shaped body, and spherical body

2-2 Marine sediments

described that egg capsules are composed of ortho-and U-shaped body without filaments from the Late

1961), but they rapidly turned black when transformed

microplankton incertae sedis, and described Beringiellamuch lighter in color. Interestingly, Harmsworth (1968)

Bujak (1984) discovered palynomorphs of dark-coloredpolyphenols and are initially white (de Beauchamp,

Pleistocene sediments of the Bering Sea, treated them as

into quinone, and Neorhabdoceles egg capsules were

fritilla as a new genus and species in Acritarcha. ThisThe oldest occurrence of fossil turbellarian egg capsules

Palaeostomocystis by Roncaglia (2004), and thencomposed of the body capsule and the operculum.

species was subsequently transferred to the genus(Gyratrix type) was reported in the Middle Pleistocene

Beringiella was identified as a junior synonym of the(ca. 250 x 10 yBP) freshwater sediments of Lake Biwa-

genus Palaeostomocystis. The genus Palaeostomocystis

3ko, central Japan by Kadota (1973).

was erected by Deflandre (1937) with the type species ofPennak (1978) illustrated two morphologically different

Palaeostomocystis reticulatum from the Cretaceous inegg capsules: one is spherical and larger (planarian

France. However, we need more careful consideration of

cocoon), and the other is ellipsoidal with an operculum

this taxonomic change, as we discuss later.

and a slender stalk (Gyratrix sp.), and both have basal

Funnel, bell, pitcher, and cup-shaped palynomorphs

attachments at the end of stalks. Pennak (1978) also

also occur in modern marine sediments apart fromlight-colored when recently deposited, but soon become

tintinnid cysts and loricae (Reid and John 1978, 1983;

mentioned that the cocoons (egg capsules) are initiallyplankton, and many of them have been classified as

dark brown or blackish. While introducing the methods

van Waveren, 1994; Mudie et al., 2010; 2011; Pieńkowski

of Quaternary palynology, Warner (1990) explained non-

et al., 2011; 2013). van Waveren (1994) morphologicallypollen palynomorphs with funnel, bell, pitcher, and cup-characterized these funnel, bell, pitcher, and cup-shaped

shaped morphologies as Neorhabdocoela (flatworm)

palynomorphs other than tintinnid, based on the caseegg capsules: Gyratrix type with a slender stalk,where Favella serrata contained a resting cyst in a lorica

Microdalyellia type, and spherical-shaped type.

shown by Reid and John (1978). van Waveren (1994)

H a a s (19 9 6 ) n a m e d N e o r h a b d o c o el a o o c y t e s

named them “tintinnomorphs” and classified them into

(turbellarian egg capsules) in gyttja sediments of

76 morphotypes and reported their occurrences in deep-

the freshwater lake "Wallisellen-Langachermoos"

sea sediments from the Banda Sea, Indonesia. Thereafter,

in Switzerland according to their mor phologicalmany researches followed the concept of tintinnomorphs.

characteristics in the process of studying them from a

Among them, Matsuoka (1994, plate II, fig. 9) illustrated

paleoecological point of view. Haas (1996) identified thea cup-shaped palynomorph furnished with a filament

following species: Microdalyyellia amigrea (Type 1A–

from surface sediments of Aso Bay, West Japan as

E), Gieysztoria virgulifera, Strongylostoma radiatum

indeterminable, slightly similar to Cretaceous acritarch(Type 1A–B), Mesostoma lingua Type, Gyratrix

Domasiella erected by Eisenak (1969).

hermaphroditus Ecotype 1A Gieysztoria virgulifera D,

Cup-shaped palynomorphs (Head 2007, fig. 12l, m)and Neorhabdocoela Unknown Type A. Gelorini et al.

occurred in the Eemian Interglacial (Late Pleistocene)in East African lake sediments to contribute to future

identified as tintinnid lorica by Head (2007). da Silva(2011) described non-pollen palynomorphs conserved

sediments collected in the Ba ltic Sea a nd werepaleoenvironmental studies. As microscopic zoologicalet al. (2017) reported the production of tintinnomorphs

remains, Gelorini et al. (2011) recorded egg capsulesin Holocene sediments collected from the Coastal

identified as Gyratrix hermaphroditus and Microdalyellia

Plain of Santa Catarina, southern Brazil. Matsuoka

amigrea of Neorhabdocoela (turbellaria). However

et al. (2017) and Matsuoka and Ishii (2018) followed

different morphotypes with in these species werethe classification of palynomorphs proposed by van

observed, and these morphotypes were regarded as not

Waveren (1994) and introduced the funnel, bell, pitcher,different species. Thus, the study of turbellarian egg

and cup-shaped palynomorphs called tintinnomorphs

capsules preserved in sediments was initially focused on

as tintinnid (Ciliata). In contrast, Mudie et al. (2020,

the Holocene freshwater sediments.

2021) recognized that tintinnomorphs also contain20

Turbellarian egg capsule as one type of aquatic palynomorph; reconsideration of Tintinnomorph

egg capsules of turbellarians that are taxonomicallydifferent from ciliate, and emphasized that caution

should be exercised in environmental assessment basedon these palynomorphs. Thus, the taxonomic position of
tintinnomorphs is now in confusion.

3. Modern turbellarian egg capsules
There are two types of turbellarian eggs, dormant(resting) and subitaneous (temporal). Dormant eggs
spend their time in a non-adaptive environment in egg

capsules and are released through the operculum whenthe environment becomes favorable.

Fig. 2 Descriptive terms for turbellarian egg capsules.

Hoang et al. (2013) called these two different types“D egg” and “S egg”. Empty egg capsules produced

Drawing of Syndesmis hermaphroditus reported byby D eggs will be preserved in sediments and remain

https://www.youtube.com/watch?v= 0eesPpts8UQ.

as fossils (e.g., Harmsworth 1968 as Neorhabdocoele

A, Egg capsule with operculum stored in the body before(?) egg capsules). According to video images https://

hatching. B, Egg capsule without operculum preserved in

www.youtube.com/watch?v =sefdjf Bmkko, a single

sediment after hatching. Note a basal attachment at theegg capsule together with stylet is observed in Gyratrix

end of the stalk.

hermaphroditus Rhrenberg, 1831. This egg capsule isbrownish in color, elongated ovoidal in shape and has aslender transparent stalk (filament-like). In another video

Syndisyrinx franciscanus Leham, 1946 have one orwatch?v= 0eesPpts8UQ), the egg capsule is yellowishof sea urchins, and then expulsed to seawater together

image of G. hermaphroditus https://www.youtube.com/

several egg capsules and are released into the intestinebrown in color, and elongated ovoidal in shape and at awith the feces. Embryos are mature in the egg capsules,

position one-fourth from the top an operculum suture candormant in the sea urchins, exposed to intestinal juice

be seen. Additionally, a rather stout stalk with a bulge

after being released into the intestine of sea urchins

can be observed. The last shot of these images, which is

to induce hatching, and hatch when released into

probably after spawning, shows a wider aperture withseawater. At the hatching, a part of the egg capsule isoperculum suture and basal attachment at the posterior

split to release embryos. After hatching, the empty egg

end of the stalk. Therefore, this egg capsule seems tocapsules are preserved in sediments. Also, the interesting

be free from a turbellarian body. Egg capsules are one

photos shown by Zapata and Várela (1981) and http://of the reproductive organs of turbellarians belonging

dorsetmicroscopy.blogspot.com/2014/07/budding-or-

to Neorhabdocoela. The egg capsule is an organ in

not.html may suggest that at the hatching, egg capsules

which a part of the vagina swells like a bag and storesattach to suitable particles such as foraminifers.

fertilized eggs there. Egg capsules contain one or moreturbellarians. In addition, on the surface of egg capsules,

3-1 Morphology of modern egg capsulesfilament) for adhering to other substances after spawning

capsule, stalk and basal attachment parts. At one-third

stalks attaching to the basal substance are sometimes

indicated by a circular suture at the spawning (Fig. 2).

there are sticky substances secreted and a stalk (orTurbellarian egg capsules consist of mainly three parts:

from cement glands (Okugawa in Ueno, 2010). Largerof the capsule from the top, an operculum is formed, as

hollow (Shinn 1985).

Most of fossilized turbellarian egg capsules extracted

Shinn (1983, 1993) described the behavior of thefrom sediments miss the operculum and form an opening

turbellarian egg capsules as follows. Most of thewhich is called an ‘aperture”. Some turbellarian capsules

umagillids that parasitize sea urchins for example,

do not have a stalk nor a basal attachment. Based on
21

Kazumi Matsuoka・Takuto Ando

Fig. 3 Six basic morphological types observed inFig. 4 Six basic morphological types of turbellarian egg

A, B, and C, Egg capsules with stalks. D, E, and F, Egg

A, B, and C, Egg capsules with stalks; D, E, and F, Egg

modern turbellarian egg capsules.

capsules preserved in sediments.

capsules without stalks. A & D, ellipsoidal type. B & E,

capsules without stalks. A and D, ellipsoidal type. B andsubspherical to ovoidal type. C & F, spherical type.

E, subspherical to ovoidal type. C and F, spherical type.

A, drawing of Wahlia pulchella egg capsule illustrated byA, modified from ELELNO-16 of van Waveren (1994,

Kozloff and Shinn (1987, fig. 2). B, drawing of Syndesmis

pl. 1, fig. 13). B, modified from T 1221 of Gelorini et al.

dendrastrosum egg capsule illustrated by Shinn (1988,(2010, plate VIII, T.1221). C, modified from Haas (1996,

fig. 2). C, drawing from Syndesmis evelinae illustrated

fig. 1 (p), Neorhabdocoela Unknown – Type A).

by Hertel and Duzynski (1991, fig. 1). D, drawing from

Gieysztoria sp. from Yamazaki (2020, frontispiece 4 C).
E, Castrella truncata illustrated by Uchida et al. (1965,

fig. 59A). F, drawing from Strongylostoma ratiatum
illustrated by Okugawa in Ueno (2010, fig. 12–28 F)

these morphological features, modern turbellarian

2-2 Spherical type e.g., Bothromesostoma personatum

1. Stalk Group

Most turbellarian egg capsules have a smooth surface;capsules are grouped as follows (Fig. 3);(Okugawa in Ueno, 2010) (Fig. 3F)

1.1. Ellipsoidal typee.g., Gyratrix hermaphroditus

however, a few have an ornamented wall, such as the

1.2. Cup-shaped typee.g., Wahlia pulchella (Kozloff(Shinn 1985) (Fig. 4).

1.3. Spherical typee.g., Syndesmis dendrastrorum(Gelorini et al., 2011) (Fig. 3A)

waving striations in Anoplodium hymanae Shinn, 1983

and Shinn, 1987) (Fig. 3B)(Shinn, 1988) (Fig. 3C)

3-2 Morphology of turbellarian egg capsulespreserved in sediments

A few r e s e a r ch e r s h ave p r o du c e d s ch em a t ic

2. Non-Stalk Groupillustrations of turbellarian eggs as introduced above(Yamazaki, 2020) (Fig. 3D, E)

and of some tintinnomorphs (van Waveren, 1994). In

2-1 Ellipsoidal/cup-shaped type e.g., Gieysztoria sp.

(Lohmann, 1910; Harmsworth, 1968; Haas, 1996)

22

Turbellarian egg capsule as one type of aquatic palynomorph; reconsideration of Tintinnomorph

Fig. 5 Possible candidate for fossil turbellarian egg

Fig. 6 Fossil and modern Palaeostomocystis sphaerica

A- C, turbellarian egg capsules found in moder nA, Palaeostomocystis sphaerica Deflandre 1937 (fig.

capsules possessing stalk with basal attachment.

Deflandre 1937.

sediments. A, drawing from Roncaglia and Kuijpers

6, holotype) from Cretaceous. B, Palaeostomocystis(2006, fig. 3e). B, drawing from Pieńkowski et al., (2011,

sphaerica Deflandre, drawing from Hartmann et al.

fig. 5i). C, drawing from Matsuoka (1994, pl. II, fig. 9).

(2018, pl. 5, fig. 22). C, Palaeostomocystis sphaerica

D, Domasiella discophora (Acritarcha) described byDeflandre, drawing from Warny (2009, pl.1, fig.6). Note:

Cookson and Eisenack (1962, pl. 7, fig. 18), which was

all specimens have a small aperture with collar.

probably shown upside down and with no aperture.

addition to Lohmann (1910), others attempted to makevery short stalk), Matsuoka et al. (2017, fig. 2l), da Silva

were illustrated on the basis of remains recovered fromand others (Fig. 5).

a systematic scheme of fossilized egg capsules. Theseet al. (2017, fig. 4B-E), Mudie et al. (2000, figs. 5, 8, 12)

modern sediments and it is very difficult to know their

The modern cup-shaped type with a long or short stalkcorresponding adult worms. On the other hand, many

is similar to (Lohmann 1910, fig. 16a, b), Harmsworth

long time ago, but not so much attention has been paid

fig. 1;n, o as Gyratrix hermaphroditus), Roncaglia andstudies of various Turbellaria have been carried since a(1968, fig. 7, 15), Zapata and Várela (1981), Haas (1996,

to their egg capsules; for example, the egg capsules

Kuijpers (2006, fig. 3e), Head (2007, fig. 12m), Gelorini

have been briefly illustrated as just ovoidal shaped with/et al. (2011, pl. viii, T. 1221), Chaweepak et al. (2019,

without stalks (filaments). In addition to this, mostfig. 2-11), Mudie et al. (2020, fig. 11-9,12), McCarthy etfossilized egg capsules preserved after hatching lose theal. (2021, fig. 5h as Gyratrix sp.), and others.

operculum and this may cause morphological changes

The modern spherical type with a stalk was illustrated

from the original shape of egg capsules. At present, it is

by Haas (1996, fig. 1p as Neorhabdocoela, Unknown).

fossilized egg capsules (Fig. 4）.

recorded in surface sediments of West Japan, and it was

impossible to identify the parent turbellaria based on theThis type with a long and flexible stalk was also
pointed out that this remain was apparently similar to

3-2-1 Stalk Groupan Acritarch Domasiella (Matsuoka, 1994, pl. 2, fig. 5).

Mainly three types of stalks can be seen on modern

However, Domasia discophorai Cookson and Eisenack,turbellarian egg capsules: filament type (rather longer

which has a subspherical to elongate body with a stalkand slender), spine type (short and stout), and short anddistally divided into two appendages, was found frombroad type. Sometimes the stalks are incomplete due toCretaceous sediments of Australia and initially describedbe cut on a way, because the attachment structures areas an Acritarch by Cookson and Eisenack (1962) All

missing.

specimens of Domasa shown by Cookson and Eisenack

The modern ellipsoidal type with stalk is identical to(1962) have no aperture at the apex. Since some of themillustrations and photographs provided by Lohmannhave one or two stalks at the antapex, a few different(1910, fig. 15b and probably fig. 15a as a complete form),

species may be included in D. discophora. Later,

Warner (1989, fig. 8a), Haas (1996, fig. 1l, m as Gyratrix

Eisenack et al. (1973) transferred them to the new genus

hermaphroditus), Hartman et al. (2018, pl. 5 fig. 17-19;

Domasiella (Fig. 6).
23

Kazumi Matsuoka・Takuto Ando

3-2-2 Non-Stalk Group

This group is also morphologically divided into three

types, like the Stalk Group.

The fossil elongate type was shown by Bujak (1984,

pl. 4, fig. 12-14 as Beringiella fritilla), Warner (1989,

Fig. 8b as Microdalyellia-type), Haas (1996, fig. 1a-f as

Microdalyellia armigera including five morphotypes),

Fig. 7 Morphological variation of Palaeostomocystis

Roncaglia & Kujijers (2006, fig. 7d-f), Warny (2009, pl.

A, drawing from Bujak (1984, pl. 4, fig 14; holotype). B,

Roncaglia (2004, fig. 2j as Palaeostomocystis fritilla),fritilla (Bujak) Roncaglia.

1 fig. 6-8), Hartman et al. (2018, pl. 5 figs. 10-13, 14-16),

drawing from Roncaglia and Kuijpers (2006, fig. 7d). C,

Gelorini et al. (2011, pl. viii, T1221, T1223), Matsuoka

drawing from Roncaglia and Kuijpers (2006, fig. 7e). D,

and Ishii (2018, fig. 4c, d), Mudie et al. (2020 fig. 14

drawing from Roncaglia and Kuijpers (2006, fig. 7f). E,

as Beringiella Bujak 1985), MacCarthy et al. (2021 as

drawing from Roncaglia (2004, fig. 2j).

Microdalyellia), Head (2007, fig. 12l) and others.

3-2-3 Beringiella or Palaeostomocystis (Table 2)

the surface decoration, the morphology of the opening

However, morphotypes of fossilized egg capsules

is significantly different between these two species.

that are mostly similar to those of modern turbellarians

The opening of Palaeostomocystis is described as a

described above are also found, and sometimes similarpore or a more-or-less large opening with or without aseveral different names. For example, the ellipsoidal(Deflandre, 1937, fig. 5) has a more-or-less largemorphotypes are classified as Acritarcha and called byvariably developed collar. The type species P. reticulata
opening. Since P. sphaerica (Deflandre, 1937, fig. 6)

type like that of Gieystoria sp. without a stalk is similar

to the acritarch genus Beringiella or Palaeostomocystis.

has a pore with collar, the structure of the openings ofBeringiella fritilla Bujak as a new genus and species

these two species is clearly different. Although a pore

was firstly described from Pleistocene marine sedimentswith collar is not known in the modern Rhabdocoela

by Bujak (1984). B. fritilla is ornamented with a thick,egg capsule, eggs produced by Trematoda (Neoophora)

species are known to be considerably smaller than the

foveolate wall with a rather wide aperture and a free
operculum (Bujak 1984). Later, Roncaglia (2004)

Turbellaria egg capsules, which are usually over 100 μm

transferred Beringiella to Palaeostomocystis, which is

and rarely less than 100 μm (57-63 x 41-50 μm for B.

also characterized by a thick, foveolate or reticulate wall

fritilla). For example, Clonorchis sinensis (Clonorchiasis), a species that has a pore with collar, is sometimes

and a rather wide aperture without a collar. Roncaglia

detected in sediments and forms residual eggs. The(2004) also described a new species, Palaeostomocystis

subtilitheca, characterized by a transparent wall andegg (30 x 16 μm) is an elongated ellipsoid with a smalllarger aperture with concentric ring, from Pleistocene

opening at the top and a collar around the opening

sediments and suggested that this palynomorph was not a(Uddin et al. 2012). Many human parasites belong toTrematoda, and their eggs have also been detected inciliate lorica but a cyst form (Fig. 7).

Palaeostomocystis is one of the organic microfossils

sediments (e.g. Kanehara and Kanehara, 1994; Le Baully

established by Deflandre in 1937. Since then, there has

et al., 2007). Some of these eggs (Diphyllobothrium

been much debated about whether Palaeostomocystissp., Fasciola sp., and Opistorchis sp.) illustrated by Le

Baully et al. (2007) have quite similar morphology ofis a dinoflagellate cyst or not. For example, Stover

Beringiella. In addition, fish schistosomiasis is known

and Evitt (1978) considered it as a dinoflagellate cyst,

however it is now treated as an Acritarch (Fensome

to be caused by a member of Trematoda (e.g., Ogawa

et al., 2019). The type species of this genus is

and Egusa, 1986; Ogawa, 2010). Therefore, it is possible

Palaeostomocystis reticulata Deflandre, but at the samethat an unknown parasite egg belonging to Trematoda

is preserved in aquatic sediments. On the other hand,time Deflandre (1937) also described Palaeostomocystis

Hartman et al. (2018) proposed that P. sphaerica mightsphaerica Deflandre as another new species. Besides

24

Rhaditophora Rahidocoela

Rhaditophora Rahidocoela

Rhaditophora Rahidocoela

Gieysztoria virgulifera Plotnikow

Strongylostoma radiatum Müller

Mesostoma lingua Abildgaad

Rhaditophora Rahidocoela

Microdalyellia sp.

25

Acritarch

Acritarch

Acritarchtintinnid
Acritarch
Acritarch
Acritarch
Acritarch
Acritarch
Acritarch

Acritarch

Acritarch

Acritarch

Acritarchtintinnid
CiliatePalaeostomocystis subtilitheca Roncaglia

Palaeostomocystis fritilla (Bujak)

Palaeostomocystis fritilla (Bujak)
Tintinnid lorica
Palaeostomocystis reteculata Deflandre
Palaeostomocystis sp. 1
Palaeostomocystis fritilla (Bujak)
Palaeostomocystis sphaerica Deflandre
Palaeostomocystis fritilla (Bujak)
Palaeostomocystis cf. firitilla (Bujak)

Palaeostomocystis cf. reticulate Deflandre

Palaeostomocystis sp. C

Palaeostomocystis sphaereica Deflandre

Palaeostomocystis sp. B
Tintinnomorph
Beringiella fritilla Bujak (possibly)*: type species for the genus Palaeostomocystis

Acritarch
Acritarch
Acritarch
Acritarch
Acritarch

Acritarch

Palaeostomocystis ovata (Wilson)

Palaeostomocystis pachtheca Cookson & Eisenack
Palaeostomocystis minor Jiabo
Beringiella fritilla Bujak
Palaeostomocystis faveolata Slimani
Palaeostomocystis globosa Louwye

Acritarch
Acritarch
Acritarch
Acritarch

Palaeostomocystis reticulata Deflandre*
Palaeostomocystis cretacea (O. Wetzel)
Palaeostomocystis sphaerica Deflandre
Palaeostomocystis punctulosa DeflandrefossilRhaditophora Rahidocoela

Gyratrix hermaphroditus Erhenberg

Rhaditophora Cestoda
Rhaditophora Cestoda

Rhaditophora Rahidocoela

Microdalyellia armigera Schmidt

Diphyllobothrium sp.
Opistorchis sp.

Rhaditophora Rahidocoela
Rhaditophora Rahidocoela

Taxonomy

Neorhabdocoele
Microdalyellia typemodernSpecies

FW sediment (Holocene)

FW sediment (Holocene)
FW sediment (Holocene)Age

operculum suturewider aperture, lack a faveolate wall;
more slender, reticulate surface-wall ornamentation,
conical antapex
one polar collared pylome
a single collared pylome, frustoconical collar; covered
with outer menbraneyellowish, ovoidal vesicle with one polar aperture

rather smaller aperture comparing with Deflandre
with callor
wider aperture
with callor

One of the poles is lost by the development of a large
aperture
wider aperture

Ovoidal to obtusi-coniform,unilayered, thin-walled
vesicle with circular to oval equatorial outline, circular
aperturefine-meshed reticulate network of muri

smaller aperture with operculum

M, sediment (Holocene)M, sediment (Holocene)

Matsuoka and Ishii 2018
Mudie et al. 2021

Hartman et al. 2018

Pienkowski et al. 2012, 2020

M, sediment (Late Pleistocene)M, sediment (Holocene)

Warny 2009

Roncaglia and Kuijpers 2006
Head 2007

Roncaglia 2004

Cookson and Eisenack 1971
Jiabo 1978
Bujak 1984
Slimani 1994
Louwye 1999

Eisenack 1971

Deflandre 1937
Deflandre 1937
Deflandre 1937
Deflandre 1941

McCarthy et al. 2021

Gelorini et al. 2011

Le Bailly et al. 2007

Haas 1996

Harmsworth 1968
Warner 1989

Reference

M, sediment (Late Pleistocene)M, sediment (Holocene)M, sediment (Late Pleistocene; Eemian)M, sediment (Holocene)

Middle Cretaceous
Paleocene (early Tertiary)M, sediment (Pleistocene)
Late Cretaceouslate Miocene

Paleocene

Cretaceous
Late Cretaceous
Cretaceous
Jurassic

FW sediment (Holocene)

FW sediment (Holocene)elongate ovoidal with polar opening; 57 x 40 µm
Archeological site (human coprolites)
elongate ovoidal with polar opening; 120 x 70 µm, 27x13 (Holocene)µm

sperical, radial operculum suture

spherical, wide aperture

truncated pyramid, wide aperture

ellipsoidal or ovoidal; width range: 70-120 µm, length
range: 100-210 µm, wide aperture: with fine operculum
sutureMorphology

similar fossils identical to the genera Beringiella and Palaeostomocystis.

Table 2 Modern turbellarian ellipsoidal to cup-shaped egg capsule in the group without stalk and morphologically1

A-E(different

Surface

Resting stage of ciliate protists

Egg capsule of turbellaria

as new combination

as new species

Transffered from Leiosphaeridia to
Palaeostomocystis.

Type species for Palaeostomocystis
Tranfered from Trachelomonas ?

Type UG-1221, UG-1222 and UG-1223 areprobably related to the oocyte types

Morphologically similar to Beringiella

Some other Mesostoma species included

Two types; 1 A-B (different Surface
ornaments)

Five types;
ornaments)

Remarks

Turbellarian egg capsule as one type of aquatic palynomorph; reconsideration of Tintinnomorph

Kazumi Matsuoka・Takuto Ando

Fig. 8 Comparison between turbellarian egg capsule (A, B) and ciliate cyst (C, D).

A, Egg capsule after hatching observed in surface sediment of Welu River estuary, Thailand. B,

Schematic illustration of egg capsule without an operculum. C, Illustration of the ciliate cyst
shown by Reid and John (1978). D, Empty ciliate cyst observed in surface sediment of Osaka
Bay, Japan.

be identical to cysts of ciliates or Perkinsozoans on theand identified them as parasitic Diphyllobothrium sp. andand Reid and John (1983). Therefore, the fact that theand Dioctophyma sp. of Tremadoda, Neoophora. Thisbasis of suggestions by Leander and Hoppenrath (2008)

Opistorchis sp. together with Taenia sp., Capillaria sp.,

opening of P. sphaerica is not similar to turbellariansuggests that morphologically similar but ecologically

egg capsules but rather to eggs of Trematoda, cysts ofdifferent eggs or egg capsules of turbellarians exist in

ciliates or Perkinsozoans suggests that P. sphaerica

sediments. Therefore, for understanding the origin of B.

may be in a different genus from Palaeostomocystis.

fritilla, further investigation of egg capsules and eggs of

Palaeostomocystis sp. C of Hartman et al. (2018) may

modern turbellaria and trematode is needed.

also be different from the genus Palaeostomocystis

4. Turbellarian egg capsule remains

because of its collared pylome. Hartman et al. (2018)as environmental indicator

described Palaeostomocystis sp. B characterized byelongate body ornamented with coarse reticulate structure
and circular aperture (Fig. 8).

According to the summary of Platyhelminthes

As discussed from the viewpoint of morphology,

provided by Norena et al. (2015), modern turbellarians

sphaerica are not ciliate cysts and is possibly identicalbrackish, freshwater, wetland, water film of moss,

species belonging to Palaeostomocystis excluding P.

inhabit extremely diverse environments: marine,

to turbellarian egg capsules. This suggestion is also

decomposed leaves, or debris, and the majority of

supported by the chemical composition of B. fritillathem are basically carnivores, but some of them areshown by Mudie et al. (2021).

ectoparasitic or symbiotic in association with otherOn the other hand, Le Baully et al. (2007) reported

invertebrates. Interestingly, egg-capsule-forming

ellipsoidal eggs morphologically similar to Beringiellaturbellarians inhabiting freshwater include both freefrom human coprolites of the Neolithic archeological sites

living and ectoparasitic or symbiotic species. Gyratrix
26

Turbellarian egg capsule as one type of aquatic palynomorph; reconsideration of Tintinnomorph

hermaphroditus, which is known to produce egg capsules

number (van Waveren, 1993) and only around 100 egg

to the Family Dalyelliidae. It is also well known

unpublished data). For understanding paleoenvironmental

from sediments, is a free living turbellarian belonging

capsules / dry sediment weight in Beppu Bay (Matsuoka,that free-living turbellarians inhabit a large number

significance of turbellarian egg capsules particularly inof sea areas, but the family Umagillidae members,marine sediments, further studies of morphology, ecology

Anoplodium hymanae, Syndesmis dendrastorum, andand physiology of each species are needed as suggested

Wahlia pulchella, which can produce egg capsules that

below.

are preserved in sediments as remains (fossils), areendosymbionts of sea cucumbers and sea urchins (Shinn,

5. Tintinnomorph problem

1985; 1986; 1988. Kozloff and Shinn, 1987) (Table 1).

Fossil turbellarian egg capsules formerly called

van Waveren (1994) proposed the term “tintinnomorph”

tintinnomorphs have so far been observed in various

for funnel-, bell-, pitcher-, and cup-shaped palynomorphs.

(van Waveren, 1994) to high latitudes (e.g., Pieńkowski

several parts and preserved in sediments, referring

environmental areas, from low latitudes (e.g., Banda Sea

It is speculated that tintinnids are decomposed into

et al., 2011; 2013; 2020, Roncaglia and Kuijpers, 2004,

to the specimen in which Favella serrata illustrated

and from freshwater (e.g., Warner, 1989; Haas, 1996;

by Reid and John (1978) contains a resting cyst in a

Gelorini et al., 2011), tidal marsh (e.g., Matsuoka etlorica. It is clear that the concept of “tintinnomorph”

al., 2017, Chaweepak et al., 2019), coast (e.g., da Silva

has been obtained by artificial combine of different

et al., 2017, Matsuoka and Ishii, 2018, Mudie et al.,components. However, these palynomorphs preserved2020) to offshore (e.g., van Waveren, 1993 Banda Sea).

in the sediment are taxonomically, ecologically andHowever, most of these reports have not identified egg

physiologically different organism remains, namely,
turbellarian egg capsules, ciliate resting cysts, andcapsules as genus or species levels, because taxonomicand ecological studies of each morphotype have been

lorica, rather than the individual parts of a ‘tintinnid’

not fully progressed. This suggests that the turbellarian

being preserved separately. Therefore, as pointed out by

egg capsules are not so helpful for paleoenvironmental

Mudie et al. (2021), the use of the term “tintinnomorphs”

reconstruction at present.

may cause confusion, when we intend to reconstruct

Since the report of Harmsworth (1968), several reports

the paleoenvironment and paleoecology based on

described the turbellarian egg-capsules from freshwater

the production of these palynomorphs. It is instead

sediments. For example, Kadota (1973) conducted

appropriate to use terms that indicate each taxon.

a paleontological study of a sediment core collected

Morphological differences between tubularian egg

from Lake Biwa-ko, Japan and reported the density

capsules and ciliate cysts are as follows:

sediment. Haas (1996) recorded 3500 oocysts / cc as the

100 μm in size (e.g., Haas, 1996; Shinn, 1985), whereasof turbellarian egg-capsules as 389 individuals / cc of

The egg capsules of modern turbellarian species are overhighest density of Gytratrix hermaphooroditus Ecotype

the size of ciliate cysts identical to Strombidium sp. is

1-A from the Holocene freshwater lake sediments nearless than 100 μm (Matsuoka and Ishii, 2018). However,Fusopsis collected from the North Sea was more than

Zürich. According to Eeckhaut et al. (2004), 128 out of
the 202 inspected sea cucumbers contained at least 6 and100 μm but furnished with cylinder-like head (Reid and

up to 10,000 egg capsules (mean of 1,433) and Doignon

John, 1978). The modern turbellarian egg capsules are

and Jangoux (2001) reported that Anopodium parasite, ofvariable from orange to brown in color, but usually lightto dark brown when they are extracted from sediments.

which the egg capsule shape had not been clearly known,

The ciliate cysts are mostly colorless and transparent.

produced 183,455 capsules per year. Thus, a considerable

number of turbellarian egg capsules seem to be produced

The structures around the hatching and germinationnear shallow coastal areas. However, in marine off-shore

apparatus are also different between turbellarian egg

sediments, turbellarian egg capsules are not dominantcapsules and ciliate cysts. Turbellarian egg capsules haveamong aquatic palynomorphs, constituting less thanan aperture with an operculum, whereas ellipsoidal to

10 individuals per sample as the originally counted

elongated ovoidal ciliate cysts have a plug and cap or27

Kazumi Matsuoka・Takuto Ando

Fig. 9 Wall ornamentation on turbellarian egg capsules.

Fig. 10 Different types (filament (A, B), spine (C, D) and

1985, fig. 10). B, vertical wavy lines of fossil egg capsule

A from Lohman (1910, fig. 15b), B from van WaverenA, vertical wavy lines of Anopodium hymanae (Shinnrod (E)) of stalks developed on turbellarian egg capsules.

of T 1224 (Gelorini et al. 2011, plate VIII).

(1994, pl. 1, fig. 13), C from van Waveren (1994, pl. 1, fig.

16), D from Gelorini et al. (2010, pl VIII, T 1221), E fromPieńkowski et al. (2011, fig. 5 i).

neck with papula (Reid and John, 1978; 1983) (Fig. 7).

independent species.

from turbellarian egg capsules, and it is recommended

6-2 Morphology of egg capsules - surface ornament

funnel-, bell-, pitcher-, and cup-shaped palynomorphs

hermaphroditus shows a world-wide distribution, but the

Therefore, it is reasonable to differentiate ciliate cysts

hereafter to use “turbellarian egg capsules” for the brown,

Ti m o s h k i n e t a l . ( 2 0 0 4 ) m e n t i o n e d t h a t G .

with or without a stalk.

wall of egg capsules of Eurasian populations is thinnerand different from others in explaining expansion of its

6. Further study for understanding

world-wide distribution. Gelorini et al. (2010) observed

turbellarian egg capsules

cup-shaped turbellarian egg capsules ornamented with

Morphology of the following features are important forlongitudinal wavy lines on their surface from modern

turbellarian egg capsules; shape, wall ornamentations,freshwater sediments. Interestingly, a similar structure

type of stalks, and a shape of basal attachments.

was also found by Shinn (1985) in egg capsules of A.
hymanae, which inhabits the coelom of a sea cucumber.

6-1 Morphology of egg capsules - their shapeThus, the surface ornament on egg capsules is also

As described above, two different types, with several

probably an important feature for species identification

subtypes, of modern turbellarian egg capsules are(Fig. 9). Many and varied cup-shaped turbellarian egg

observed. However, further morphological studies arecapsules have been illustrated based on specimens

needed because insufficient data has been obtained

extracted from sediments; however, it is possible thatfor considering variations within a species. Haas

they may have been ellipsoidal before hatching and(1996) illustrated several different morphotypes called

then became cup-shaped after hatching because a larger“ecotypes” or “types” in a single species. For example,

aperture was partially formed.

four Ecotypes with different shape of capsules andsurface ornaments furnished with filament-like stalks

6-3 Morphology of stalks

types possessing different shapes of capsules and surface

capsules can be observed regarding whether they do

It is possible that these different types may represent

egg capsule with a filament-like stalk, when it is in thewere described for Gyratrix hermaphroditus and fiveAs explained above, two groups of turbellarian egg

ornaments without stalks for Microdalyellia armigera.

or do not possess a stalk. G. hermaphroditus has an28

Turbellarian egg capsule as one type of aquatic palynomorph; reconsideration of Tintinnomorph

Fig. 11 Basal attachments developed in turbellarian egg capsules.

A–C, modern capsule eggs. D-E, fossil capsule eggs preserved in sediments. A, Aegla

serrana (Amato et al. 2003, fig. 4). B, drawing from http://dorsetmicroscopy.blogspot.
com/2014/07/budding-or-not.html. C, Gyratrix sp. probably with operculum (Pennak

1978, fig. 82A). D, drawing from Roncaglia and Kuijpers (2006, fig. 3e). E, drawing
from Pieńkowski et al. (2011, fig. 5i). F, drawing from Matsuoka (1994, pl. II, fig. 9).

Fig. 12 Modern turbellarian egg capsules preserved in surface sediments collected from various regions.

A, Elongated capsule and long solid stalk furnished with a small basal attachment; a, enlargement of basal

attachment, loc. Lake Nakaumi, Japan. B, Cup-shaped egg capsule and stalk with small bulge (arrow) andbasal attachment, loc. Welu River estuary, Thailand. C, Conical egg capsule and slender stalk with tiny basal

attachment, loc. Manjung River estuary, Malaysia. D, Conical egg capsule and stalk with bulge and larger
basal attachment, loc. Osaka Bay, Japan. E, Conical egg capsule and long stalk, loc. Osaka Bay, Japan. F,
Two-headed egg capsule and stalk, loc. Chanthburi River estuary, Thailand. G, Vase-shaped capsule and shortstalk, loc. Chanthburi River estuary, Thailand. H, Ellipsoidal capsule with narrower aperture, loc. Osaka Bay,

Japan. I, Ovoidal egg capsule with wider aperture loc. Osaka Bay, Japan. J, Ellipsoidal egg capsule with wider
aperture, loc. Osaka Bay, Japan. K, Ovoidal egg capsule with narrower aperture, loc. Osaka Bay, L, Sphericalegg capsule with wider aperture, loc. Osaka Bay, Japan. Scale bar = 20 μm, except for A = 5 μm.
29

Kazumi Matsuoka・Takuto Andoturbellarian body. On the other hand, another Gieysztoria

foraminifera shells, and plant fragments and others as

not have any stalk. In addition to this, some groups

suggest that after being released from the body to outside,

sp. described by Yamazaki (2020 frontispiece 4C) does

illustrated by Brusca et al. (2016, fig. 10.23). This may

bearing a stalk have various basal attachments, which isegg capsules change their morphology by developing

possibly dependent on the nature of substrates that the

stalks and apertures, similarly to the change of theegg capsules attach to after they are released from thecolor of the egg capsules. Shape, color, stalks, surface

body. We need further investigation for understanding theornaments and basal attachment of egg capsules should

nature of these basal attachments (Fig. 10).

be investigated in more detail. Such further studies areneeded to understand the significance of turbellarian egg

6-4 Morphology of basal attachment (Fig. 11)

capsules as aquatic palynomorphs.

In the group of turbellarians whose egg capsules havestalks, a basal attachment can probably be confirmed

Acknowledgements

at the trailing end of the stalk, as well as formation ofan aperture in the egg capsule after spawning. It can be

The author thanks to Dr. M. Yamazaki for kindlyinferred that the basal attachment is formed because theproviding introduction and useful literatures about

to the substrate before spawning. The morphology ofkind and fruitful discussions of turbellarian egg capsules

egg capsule is released from the body and then adheres

modern turbellarian egg capsules, to Dr. P.C. Reid for his

the basal attachment is also diverse, and may depend

and ciliate cysts, and to Dr. P. Mudie for her kindon the substrate to which the egg capsule is attached.

suggestions of tintinnomorphs preserved in sediments.

For example, Zapata and Várela (1981) reported an egg

Dr. K. N. Mertens and anonymous reviewers kindly

capsule attached to the benthic foraminifera Buccellaprovide useful and constructive suggestions and criticism

which are very useful for improve of the manuscript. We

frigida. In palynological analysis, mineral particles are

dissolved during the treatment process, so it is consideredalso thanks to them. This work is partly supported fromthat the substrate to which the egg capsule is attached has

Kakenhi Grant No. 20K04089 and 21H01170.

been removed. Based on this premise, it will be a futuretask to clarify the correspondence between the substrate

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