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Gastropod parasitism on Late Cretaceous to Early Paleocene holasteroid

echinoids – Evidence from Oichnus halo isp. n.

Article in Palaeogeography Palaeoclimatology Palaeoecology · December 2009

DOI: 10.1016/j.palaeo.2009.09.010

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 Palaeogeography, Palaeoclimatology, Palaeoecology 284 (2009) 115–119

Contents lists available at ScienceDirect

Palaeogeography, Palaeoclimatology, Palaeoecology

j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / p a l a e o

Gastropod parasitism on Late Cretaceous to Early Paleocene holasteroid

echinoids — Evidence from Oichnus halo isp. n.
Christian Neumann a,⁎, Max Wisshak b
a
Museum für Naturkunde Berlin, Invalidenstraße 43, D-10115 Berlin, Germany
b
GeoZentrum Nordbayern, Universität Erlangen-Nürnberg, Loewenichstr. 28, D-91054 Erlangen, Germany

a r t i c l e i n f o a b s t r a c t

Article history: The new combined attachment and feeding trace fossil Oichnus halo isp. n. is described from oral surfaces of
Received 20 April 2009 Campanian and Danian Echinocorys tests. It shows striking conformity with traces produced by Recent eulimid
Received in revised form 3 September 2009 gastropods of the genus Thyca parasitising the asteroid Linckia laevigata. The trace is characterised by a central
Accepted 10 September 2009
penetration surrounded by the eponymous circular groove. The occurrence of Oichnus halo isp. n. in the
Available online 25 September 2009
Campanian is contemporaneous with the first appearance of eulimid gastropods in the fossil record and
Keywords:
indicates that the eulimid–echinoderm parasitic interaction was already established in the Late Cretaceous.
Parasitism © 2009 Elsevier B.V. All rights reserved.
Bioerosion
Trace fossil
Oichnus halo
Eulimidae
Thyca
Echinoids
Echinocorys

1. Introduction
The prosobranch gastropod family Eulimidae is a diverse group of
highly specialised gastropods comprising about 1500 extant species
which exclusively parasitise echinoderms (Lorenz, 2005). Within this
clade, very different strategies have been evolved to exploit host
resources. While most eulimids are ectoparasitic, living permanently
attached to a single host and feeding on mucus or host epithelium,
others live embedded within the host tissue or skeleton and dwell
in galls, or they have a true endoparasitic mode of life (Combes, 2005).
A number of ectoparasitic eulimids penetrate the host skeleton and
induce their prolonged proboscis to feed on internal tissues or
nutritive fluids. Those strategies where a modification of the host
skeleton is involved are potentially preserved in the fossil record as
trace fossils and regeneration structures.
Eulimids probably evolved at the end of the Mesozoic era. Due to
their small size (2–14 mm) and the aragonitic nature of their shell,
eulimids have a relatively poor fossil record and are not known from
facies where aragonite dissolution is prevalent. Pre-Eocene reports are
Abbreviations: MB.E, Museum für Naturkunde Berlin, Echinoderm collection; NRM,
Naturhistoriska Riksmuseet Stockholm.
⁎ Corresponding author. Tel.: +49 30 20938589; fax: +49 30 20938868.
E-mail address: christian.neumann@mfn-berlin.de (C. Neumann).
scarce and assignment to the eulimid family often doubtful. The first
occurrence of eulimid body fossils is reported from the Late Cretaceous
Coffee Sand Formation, USA (Sohl, 1964), which is of Late Campanian
to Early Maastrichtian age (Tschudy, 1975; Harrison and Litwin,
1997). Other reports from the Cretaceous are few: Sohl (1964) and
Tracey et al. (1993) describe eulimids from the Ripley Formation
(Maastrichtian, USA), and Sohl (1967) mentions eulimids from the
Late Cretaceous of New Mexico.
So far no fossil eulimids have been found together with their hosts
and the symbiotic relationship can only be inferred from trace fossils
reflecting their parasitic behaviour. These traces include attachment
scars, borings, or host-tissue responses such as swellings, galls or
regeneration features. However, most eulimid traces lack diagnostic
characters and recognition and interpretation remains difficult. In
fact, many traces of unknown origin found on echinoderms have
been referred to eulimid activity, but these interpretations often are
problematic (e.g., Kier, 1981; Alekseev and Endelman, 1989). Never-
theless, at least one eulimid genus does produce diagnostic traces.
Thyca (Köhler and Vaney) is an ectoparasite which lives permanently
anchored on the surface of its host. In this genus, an attachment organ
has been evolved from the pseudopallium (mouth sheath) that is
centred by a projecting and strongly developed proboscis and which
penetrates through the host skeleton to suck nutritive fluids. Herein,
we describe a new trace fossil ichnotaxon found on Late Cretaceous to
Early Paleocene echinoids of the genus Echinocorys Leske (Holasteroida)

0031-0182/$ – see front matter © 2009 Elsevier B.V. All rights reserved.
doi:10.1016/j.palaeo.2009.09.010
116 C. Neumann, M. Wisshak / Palaeogeography, Palaeoclimatology, Palaeoecology 284 (2009) 115–119

Table 1
Provenance and numerical data for seven Oichnus halo isp. n. on three Echinocorys tests. Number of traces refers to the lettering in Figs. 1A and 2A.

Species Locality Stratigraphy Inventory # L W H Number Max. Max. diameter Comment

(mm) (mm) (mm) of trace diameter of penetration
(mm) (mm)

Echinocorys conica (Agassiz) Lägerdorf, Germany Conica / papillosa -Zone MB.E 2342 57.8 46.7 49.7 1 7.3 1.3 Holotype
2 7.6 1.6 Paratype
3 6.9 1.1 Paratype
4 8.3 0.8 Paratype
Echinocorys conica (Agassiz) Höver, Germany Conica / papillosa -Zone MB.E 6568 55.0 47.2 49.1 1 4.5 1.1 Paratype
2 6.0 (4.5)
Echinocorys obliqua (Nilssohn) Limhamn, Sweden Danian, Paleocene NRM Ec28420 41.0 37.0 32.8 1 19.0 0.7

that exhibit a remarkable resemblance to attachment scars and
predatory penetrations formed by Recent Thyca on starfish.
2. Materials and methods
Our query for parasite traces focused on the echinoid genus Echi-
nocorys, a common epifaunal deposit-feeding echinoid with a
worldwide distribution known from Turonian to Paleocene strata.
The applicability of Echinocorys as a model taxon for the study of
parasitism in deep time has been emphasised in case studies by
Neumann and Wisshak (2006) and Wisshak and Neumann (2006).
We examined more than 7000 Echinocorys specimens obtained by
own fieldwork in the chalk of northern Germany as well as collection
specimens housed at the Museum für Naturkunde Berlin, Geologisk
Museum Copenhagen and Naturhistoriska Riksmuseet Stockholm. Our
query resulted in the recognition of 7 traces described herein which were
observed on the surface of three echinoid tests (see Table 1). These are
one Echinocorys conica (Agassiz) from the Campanian chalk of Lägerdorf,
N-Germany (MB.E 2342; Fig. 1), another Echinocorys conica from the
Campanian marly limestone of Höver near Hannover, Germany (MB.E
6568; Fig. 2A–B), as well as one Echinocorys obliqua (Nilssohn) from the
Danian chalk of Limhamn in Sweden (NRM Ec28420; Fig. 2C–D) (see
Table 1). The Recent counterpart is found on the asteroid Linckia laevigata
(Linnaeus) from the Philippines archipelago (MB.E 6569; Fig. 3). Digital
photography was undertaken after coating with ammonium chloride in
order to bring out details of ornament. Measurements of the test
dimensions and maximum width of the traces and their central
penetration were taken with the aid of precision sliding callipers.

Fig. 1. A, Oral view of Echinocorys conica (MB.E 2342) from the Campanian of Lägerdorf, Germany, featuring the holotype trace (1) of Oichnus halo isp. n. alongside three paratype
traces (2–4). B, Close-up of holotype trace, showing the circular central penetration and diagnostic circular groove (‘halo’) with corroded tuberculation within. C, Close-up of two
paratype traces (2–3), featuring regeneration textures.
 C. Neumann, M. Wisshak / Palaeogeography, Palaeoclimatology, Palaeoecology 284 (2009) 115–119
Fig. 2. A, Oral view of Echinocorys conica (MB.E 6568) from the Campanian of Höver, Germany, bearing two Oichnus halo isp. n. traces (1–2). B, Close-up of the fourth and smallest
paratype trace (1); halo partly eroded. C, Oral view of Echinocorys obliqua from the Danian of Limhamn, Sweden, exhibiting the largest O. halo isp. n. D, Close-up of large O. halo isp. n.
with atypical irregular margin and stereom degradation within.
3. Systematic ichnology
3.1. Ichnogenus Oichnus Bromley, 1981
Emended diagnosis: Circular, subcircular, oval or rhomboidal
solitary holes or pits of biogenic origin in hard substrates, commonly
perpendicular to subperpendicular to substrate surface. The holes
pass directly through substrate as a penetration, whereas the pits end
within the substrate as a shallow to moderately deep depression or
short subcylindrical pit, commonly with a depth:width ratio of 1, with
or without a central boss (in Nielsen et al., 2003).
3.2. Oichnus halo isp. n.
Plate 1, Figs. 1–3.
“Lesion made by Thyca” Elder 1979: 374–375, plate 1b.
“Circular impression and borehole caused by Thyca pellucida”
Janssen 1985: 553–560, Figs. 2C, 3C–D.
Diagnosis: Central hole with parallel smooth walls (pit in case of
incomplete penetration) surrounded by one or more circular
depressions.
Differential diagnosis: Oichnus halo isp. n. isp differs from all other
Oichnus ichnospecies by the presence of a circular groove surrounding
the central pit or penetration. The new ichnospecies is distinguished
from the closely related ichnospecies Allenusichnus circularis Santos,
Mayoral and Muñiz, 2003 and A. undularis Santos, Mayoral and Muñiz,
2003 as well as Centrichnus concentricus Bromley and Martinell, 1991 by
the presence of a central penetration in mature and non-healed traces.
Etymology: hálōs, Greek = halo (ring-shaped optical phenomenon
around sun or moon).
Type material, locality and horizon: The holotype trace (Fig. 1A: 1
and 1B) is one of 4 traces situated on the plastron of an Echinocorys
117
conica (MB.E 2342) from the conica/papillosa — Zone (Late Campa-
nian) collected at the chalk quarry “Heidestrasse” in Lägerdorf near
Itzehoe in northern Germany. Paratypes are the other three traces
found on the same echinoid test (Fig. 1A: 2–4 and 1C) and one trace
found on another Echinocorys conica (MB.E 6569), from the same
biozone of Höver in northern Germany (Fig. 2A: 1 and 2B; see Table 1).
Description: The oral side of the Echinocorys conica specimen
bearing the holotype exhibits 4 traces ranging from 6.9 to 8.3 mm in
maximum diameter (Fig. 1; see Table 1 for numerical data) with a
central, steep-walled penetration of 0.8 to 1.6 mm in diameter,
respectively. Two of these traces show signs of regeneration in the
form of tubercle formation (Fig. 1C) and, in one case, the central
penetration was closed by the healing process (left in Fig. 1C). The
diagnostic halo is a circular shallow depression surrounding the
central to slightly offset penetration. In non-regenerated traces, the
area between the halo and the central penetration appears smooth
with removed tuberculation (e.g., Fig. 1C).
Another paratype of only 4.5 mm in diameter was found on the
oral surface of the second Echinocorys conica specimen alongside a
further trace with atypically large and healed central penetration
(Fig. 2A–B). The largest recorded trace measures 19.0 mm and was
found on an Echinocorys obliqua corona, again situated on the oral
surface (Fig. 2C–D). In contrast to the holotype specimen, this trace
shows several additional concentric scars, surrounding the main
diagnostic groove, and has a slightly undulating outline. A ca. 4 mm
wide depression is developed around the central penetration. The
latter echinoid does not show regeneration textures on the trace but
signs of skeletal necrosis are visible.
Provenance and stratigraphic range: Late Campanian to Danian of
northern Germany and southern Sweden. Recent equivalents are
known throughout the tropical Indo-Pacific where they occur
exclusively on starfish hosts.
118 C. Neumann, M. Wisshak / Palaeogeography, Palaeoclimatology, Palaeoecology 284 (2009) 115–119
Fig. 3. A, Arm of the Recent asteroid Linckia laevigata (MB.E 6569) from the Philippines
archipelago showing infestation by the eulimid gastropod Thyca crystallina next to the
ambulacral furrow. B, removal of T. crystallina reveals combined attachment and
feeding trace closely resembling the fossil Oichnus halo isp. n.
4. Discussion and conclusions
The fossil traces perfectly match eulimid gastropod traces pro-
duced by the extant genus Thyca parasitising exclusively asteroids
such as Linckia (Valvatida, Ophidiasteridae) (e.g., Janssen, 1985) as
illustrated in Fig. 3. This strongly suggests that the fossil trace Oichnus
halo isp. n. has also been produced by a Thyca-like gastropod. Six
extant species of Thyca are known (Warén, 1980), all of which are
distributed in tropical Indo-Pacific shallow waters, except for the
subgenus Thyca (Kiramodulus), which occurs also in greater depths
(100–200 m). As in many other marine parasite groups, only the
females of Thyca are parasitic whereas the males are free-living
(Warén, 1983). In adult females, the foot is reduced and the snout is
strongly enlarged and has changed into a specialised attachment
organ, the pseudopallium (Fig. 4). The combined attachment/feeding
traces produced by the best-studied species, T. crystallina (Gould), are
near-circular depressions surrounding a deep central to eccentric hole
through which the long proboscis penetrates into the hosts' body
cavity. The circular depressions on the surface of the host correspond
to the margin of the pseudopallium and not to the shell's edge. The
central borehole has the shape of an asymmetrical tube with rather
smooth walls. The attachment disc is permanently fused with the
tissue of the host. Its surface is covered with an adhesive epithelium
covered with intracellular tonofibrils and microvilli which digest the
host epithelium and etch the host skeleton (Lützen and Nielsen, 1975;
Elder, 1979). Consequently, sclerites which were covered by the
pseudopallium show signs of calcite dissolution. A radula is missing in
Thyca, so boreholes must be made by enzymatic digestion. The female
proboscis extends from the centre of the attachment disc and
penetrates the test to terminate within the perihemal system near
the radial hemal strand which serves as a source of nutrients (Janssen,
Fig. 4. Schematic sketch illustrating Thyca parasitising on its echinoid host (Thyca soft
body organisation modified after Sarasin and Sarasin, 1887). Note the pronounced
proboscis penetrating through the test into the host's coelomic cavity and the marginal
fold of the pseudopallium forming the diagnostic circular groove.
1985; Egloff et al., 1988). The conspicuous trace which results from
Thyca's combined attaching and drilling behavior is unique among
eulimid gastropods and no other marine organisms living attached to
hard substrates (including host organisms) are known to produce
comparable traces (Bromley and Heinberg, 2006).
In Echinocorys, infestation rates by Thyca-like parasites were very
low (<0.05%) as illustrated by the rarity of findings. Infestation
intensity, in contrast, is high, as recorded by the number of attach-
ment traces (up to 4) on a separate host, each one inevitably produced
by a single individual since Thyca cannot change its position when
finally settled (Elder, 1979). For Thyca crystallina, Elder (1979)
reported infestation rates varying from 37% to 87% according to the
habitat type in a host population of Linckia laevigata from Banda
Island, Indonesia. Infestation rate and intensity both increased with
water energy but may also vary between Thyca species and is for
instance always lower in Phataria unifascialis (Gray) hosts with single
T. callista infestation than in L. laevigata with many T. crystallina
parasites (Salazar and Reyes Bonilla, 1998; Elder, 1979).
Oichnus halo isp. n. is exclusively found on the oral surface of its
Echinocorys host, paralleling the attachment strategy and microhab-
itat preference of most extant Thyca species. Juvenile T. crystallina
generally settle on the aboral (upper) surface of their host and
subsequently migrate towards the (lower) oral surface where they
firmly attach. The preference of the lower surface can be regarded as
an adaptation to protect the animal from predators, whereby the
patelliform shape of the shell may be an adaptation to reduce friction
against the substrate (Warén, 1983).
The occurrence of Oichnus halo isp. n. in the Campanian is con-
temporaneous with the first appearance of eulimid body fossils (Sohl,
1964). In modern seas, Thyca exclusively utilises asteroids as hosts
and cases of echinoid infestation are not known. This suggests at least
a restriction on asteroids as preferred hosts, but host switching from
echinoids towards asteroids during the Cenozoic also needs to be
considered. However, based on negative evidence from the limited
fossil record of articulated starfish skeletons, we cannot exclude that
already in the Cretaceous, Thyca utilised asteroids as hosts. Extant
species of Thyca are exclusively distributed in the tropical Indo-Pacific
where almost all of them (with exception of the subgenus Kiramo-
dulus) live in shallow waters. The present fossil evidence, however, is
from the temperate Proto-Atlantic (North Sea Basin) and from open
shelf settings.
 C. Neumann, M. Wisshak / Palaeogeography, Palaeoclimatology, Palaeoecology 284 (2009) 115–119
Unlike all other established Oichnus ichnospecies, Oichnus halo isp.
n. is a combined attachment and feeding trace and reflects the
parasitic life-style of its producer. Due to its distinct morphology it is
possible to refer it to the activity of a peculiar eulimid gastropod. This
is not only one of the oldest (although indirect) records of the family
Eulimidae, but also evidence that they were already parasitizing
echinoderms in the Cretaceous.
Acknowledgements
We are most grateful to Christina Franzén (NRM Stockholm) for the
loan of material in her care. Anders Warén (NRM Stockholm) provided
literature and is acknowledged for the fruitful discussions. Joachim
Gründel (Berlin) and Alexander Nützel (Bayerische Staatssammlung
Munich) provided valuable hints on the fossil record of eulimid
gastropods. We would like to thank Mark A. Wilson (Department of
Geology, The College of Wooster, Ohio) and Richard G. Bromley
(Geologisk Museum, Copenhagen) for their input and pertinent
comments on an earlier draft. This project is financially supported by
the European Union funding program SYNTHESYS (DK-TAF – 2388;
SE-TAF – 1753).
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