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ParasitismversusCommensalism:thecaseof
Tabulateendobionts
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[Palaeontology, Vol. 50, Part 6, 2007, pp. 1375–1380]
PARASITISM VERSUS COMMENSALISM: THE CASE
OF TABULATE ENDOBIONTS
by MIKOŁAJ K. ZAPALSKI
Laboratoire de Paléontologie stratigraphique FLST & ISA, UMR 8014 du CNRS, 41 rue du Port, F-59046 Lille cedex, France, and Warsaw University, Faculty of
_
Geology, Zwirki
i Wigury 93, 02-089 Warszawa, Poland; e-mail: [email protected]
Typescript received 6 January 2005; accepted in revised form 10 November 2006
Tube-like traces of organisms belonging to the
ichnogenus Chaetosalpinx Sokolov have been considered in
the literature as commensal endobiontic organisms of tabulate corals. Their position between the corallites (or sometimes within the septa), perforation of the host’s skeleton
and soft tissue, modification of its phenotype and a possible
inhibition of its growth show that the relationship between
these organisms and tabulate corals can best be interpreted
Abstract:
Tabulate corals are sometimes associated with other
organisms. Goldfuss (1829) described and illustrated the
tabulate coral Pleurodictyum problematicum associated
with the polychaete worm Hicetes. This association was
described later by, for example, Milne-Edwards and
Haime (1851), Schlüter (1889), Schindewolf (1959) and
Plusquellec (1965). Sokolov (1948), based on the material
from the Silurian of Fergana, described other organisms
that usually occur between the corallite walls. He considered them to be commensals of corals. In the same paper
and subsequently (e.g. Sokolov 1962) he described a few
similar genera of unknown affinities (regarded by Howell
1962 as serpulids), for example: Camptosalpinx Sokolov,
1948, Chaetosalpinx Sokolov, 1948, Phragmosalpinx Sokolov, 1948 and Actinosalpinx Sokolov, 1962 from the Devonian of different regions of the former Soviet Union (e.g.
Ural Mountains, Novaya Zemlya, Altai Mountains and
Tian-shan; Tapanila 2002 considered Camptosalpinx to be
a synonym of Chaetosalpinx). Following these publications, other researchers made additional important observations and described new taxa from the Ordovician of
Ontario and Anticosti Island, Canada (Tapanila 2002,
2004), Silurian erratic boulders of Groeningen, the Netherlands (Stel 1976), and the Devonian of the Armorican
Massif, France (Plusquellec 1968a), Asturias, Spain (Oekentorp 1969), and the Graz region, Austria (Hubmann
1991). Hill (1981) reviewed these organisms, and more
recently Tapanila (2005) published a detailed synopsis of
nearly all them. He stated that they often inhibited the
host’s growth. However, his material does not prove this,
even though it is shown on his text-figure 1.
ª The Palaeontological Association
as parasitism rather than commensalism, as previously suggested. Such an interpretation may be extended to the ichnogenera Helicosalpinx Oekentorp and Actinosalpinx Sokolov,
which show identical placement within the host colony and
similar features, such as the absence of their own wall.
Key words: Anthozoa, Tabulata, corals, parasitism, commensalism, palaeoecology.
The most common hosts of these endobionts are the
tabulate genera Favosites, Pachyfavosites and Alveolites. Up
to now, six ichnogenera of tabulate endobionts are known
(for a full list of these and their hosts, see Tapanila 2005).
Their diameters range from 0Æ1 up to c. 5 mm, but never
exceed that of the host corallite. The ichnogenera Chaetosalpinx Sokolov, Helicosalpinx Oekentorp and Actinosalpinx Sokolov do not possess their own walls.
The aim of this paper is to examine the nature of relationships between tabulate corals and some of these
organisms again, and in detail. This study is based mainly
on a review of published data on endobionts of tabulate
corals. It is, however, supported by an analysis of Chaetosalpinx ferganensis Sokolov infesting Favosites goldfussi
d’Orbigny, 1850. The conclusions drawn may also be
applied to Helicosalpinx and Actinosalpinx, which have
similar characteristics.
MATERIAL AND METHODS
The material of Chaetosalpinx ferganensis infesting Favosites
goldfussi comes from the claystones of the Grzegorzowice
Formation (Emsian ⁄ Eifelian, serotinus–partitus conodont
zones), trench 3a, Grzegorzowice, Holy Cross Mountains,
Poland. The Grzegorzowice Formation (c. 160 m thick)
consists mainly of claystones, mudstones, marls and limestones (Malec and Turnau 1997; Halamski and Racki 2005;
Malec 2005 for detailed stratigraphy; Zapalski 2005 for a list
of tabulate corals occurring in this formation and a map
showing the locality). The specimens discussed here were
doi: 10.1111/j.1475-4983.2007.00716.x
1375
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PALAEONTOLOGY, VOLUME 50
collected during the 1950s from trenches dug north of the
village of Grzegorzowice. They were used by Stasińska
(1958) for her taxonomic work on F. goldfussi (F. goldfussi
eifeliensis in her paper), in which she only mentioned the
presence of ‘commensal organisms’. I collected one additional corallum in the summer of 2006. Altogether eight
thin sections were prepared for this study. Two thin sections from Stasińska’s collection without detailed labels
were also used; these are transverse sections of F. goldfussi,
also containing numerous C. ferganensis, and most probably come from the same locality.
The material is housed in the Institute of Palaeobiology, Polish Academy of Sciences (Warsaw; institutional
abbreviation ZPAL) and in the Faculté Libre des Sciences
et Technologies, Lille (institutional abbreviation GFCL).
SYSTEMATIC PALAEONTOLOGY
Ichnogenus CHAETOSALPINX Sokolov, 1948
Type ichnospecies. Chaetosalpinx ferganensis Sokolov, 1948 from
the Silurian of Fergana, Uzbekistan.
Diagnosis. See Tapanila (2002).
Chaetosalpinx ferganensis Sokolov, 1948
Text-figure 1
* 1948 Chaetosalpinx ferganensis Sokolov, p. 106, textfigs 1–2.
. 1958 [undescribed]; Stasińska, pl. 3, figs 1–2; pl. 4,
figs 2, 4.
? 1969 Chaetosapinx? cf. ferganensis Sokolov; Oekentorp,
p. 193, text-fig. 8, pl. 13, figs 1–4; pl. 16, fig. 4.
1976 Chaetosalpinx huismani Stel; Stel, p. 738, textfigs 4, 9–11.
1976 Chaetosalpinx groningae Stel; Stel, p. 741, textfig. 12.
2002 Chaetosalpinx ferganensis Sokolov; Tapanila, p. 111,
text-fig. 2
Material. Two coralla of Favosites goldfussi, one discoidal,
measuring c. 125 · 140 · 60 mm, the other bulbous columnar,
measuring c. 71 · 52 · 66 mm, both heavily infested by Chaetosalpinx ferganensis; Emsian (serotinus–partitus conodont zones),
Grzegorzowice Formation, Grzegorzowice, Holy Cross Mountains,
Poland. ZPAL T.2. ⁄ 22 (Stasińska’s collection), ZPAL T.2 ⁄ TS 1
and T.2 ⁄ TS 2 (two unmarked thin sections from Stasińska’s collection, probably from the same locality) and GFCL 2174.
Description. Small tubular structures occurring within the walls of
F. goldfussi. They are round or slightly oval in cross-section,
0Æ12–0Æ22 mm. In longitudinal section their length reaches 5 mm.
Internal structures do not occur. The tubes are filled by sparite.
Remarks. Tapanila (2002) included C. groningae Stel and
C. huismani Stel within the synonymy of C. ferganensis.
The material presented here does not show any significant
difference from the specimens described by Sokolov
(1948), Stel (1976) and Tapanila (2002); it may, however,
be noted that diameters of the individuals discussed here
show little variation.
Occurrence. Worldwide distribution (Uzbekistan, Poland, Netherlands, France, Spain, Canada), Silurian–Devonian.
ECOLOGICAL INTERACTIONS
BETWEEN THE HOST AND
ENDOSYMBIONT
The most commonly suggested relationship between the
organisms referred to above and the infested corals has
been commensalism (e.g. Sokolov 1948; Plusquellec
1968a, b; Oekentorp 1969; Tapanila 2004). Stel (1976)
mentioned a ‘parasitic symbiosis’ (¼ parasitism) but did
not present any arguments to support this. Tapanila
(2005) used the term ‘endosymbiont’ following Taylor
and Wilson (2003). This term has a very broad meaning
and does not suggest anything regarding the nature of
ecological relationships between the organisms. I presented the first arguments in favour of parasitism 3 years
ago (Zapalski 2004).
Ecological interactions: definitions
Symbiosis. The term ‘symbiosis’ was used by de Bary
(1879) to denote all interactions, but this usage seems to
be obsolete today (Goff 1982). In its more restricted sense
(also called mutualism) it is considered to be an interaction between two organisms for their mutual benefit, and
this definition is currently in common use (Krebs 2001).
Commensalism. In the older literature the broadly
accepted definition of commensalism was the relationship
between two different organisms when one receives benefits from the other without damaging it. However, in
modern ecology handbooks (e.g. Krebs 2001) it is no
longer used because it seldom occurs in nature. The scarcity of commensalism results from the difficulty of strictly
applying the definition; nevertheless, it seems to be common among a few groups of organisms, such as hermit
crabs (Williams and McDermott 2004). Symbiotic and
parasitic relationships having only a slight positive or
negative effect on one of the organisms may be described
as commensalism, but such interactions are very rare
because a loose relationship between organisms is unlikely
to be neutral for them.
ZAPALSKI: PARASITISM VERSUS COMMENSALISM IN TABULATE CORALS
Parasitism. Parasitism is a way of living in which one
organism, the parasite, uses another organism of a different species, the host, both as a habitat and a food source
(Read 1972). This interaction is positive for the parasite
and negative for the host. Combes (2001) added long
duration as an important aspect of this interaction.
1377
2000a, b). The coverage of the skeleton by soft tissue in
tabulate corals has been discussed and illustrated by several authors (e.g. Swann 1947; Schouppé and Oekentorp
1974; Plusquellec 1992, 1993). On the basis of modern
analogies and the opinions of Swann (1947) and Plusquellec (1992, 1993), it is assumed here that the skeleton
of the favositid colony was continuously covered by soft
tissue (contra Schouppé and Oekentorp 1974).
The relation between the soft tissue and the skeleton
As the endobionts occur within the skeletal tissue of tabulate corals, the relationship between the soft tissue and the
hard parts in these corals seems to be crucial. As noted
above, these endobionts occur mainly within the coralla of
favositids (with cerioidal coralla), but they are also found
within the sarcinulids (with facelo-cerioid coralla).
Nearly all modern cerioid and meandroid scleractinians
have continuous soft tissue on the skeleton (e.g. Veron
Given the position between the corallites (sometimes
within the septa) and the absence of a wall produced by
the infesting organism, it is evident that these organisms
perforated the soft body of the coral colony. After perforation and settlement on the hard part of the host, the
organism was surrounded by the growing walls of the
B
1 mm
500 µm
A
The relationship between the host and the endobiont
200 µm
E
1 mm
D
C
1 mm
T E X T - F I G . 1 . Chaetosalpinx ferganensis Sokolov (marked by arrows) on Favosites goldfussi; Grzegorzowice, Holy Cross Mountains,
Poland; Emsian. A, general view, transverse section. B, detailed view of two individuals, transverse section. C, general view,
longitudinal section. D, detailed view of one individual, transverse section. E, general view, transverse section. Abbreviations: ch,
geometry of wall changed as a result of the infestation; uc, geometry unchanged, normal corner of the corallite. A–D, specimen ZPAL
T.2 ⁄ 22; E, specimen ZPAL T.2 ⁄ TS1.
1378
A
PALAEONTOLOGY, VOLUME 50
B
C
D
E
T E X T - F I G . 2 . A scheme for the settling of the infesting organism. A, uninfested colony, longitudinal section. B, perforation of the
soft tissue by infesting organism, longitudinal section. C, infested colony after a certain length of time; compare the right corallite wall
(top) with Text-figure 1C, indicated by ‘ch’. D, transverse section of infested junction of three walls; compare with Text-figure 1E,
indicated by ‘ch’. E, transverse section of uninfested wall junction; compare with Text-figure 1E, indicated by ‘uc’.
host coral (compare Text-figs 1 and 2, the latter being a
graphic model explaining the process). In this case a normal, double wall with a cavity is observed in transverse
section (Text-figs 1, 2C–D). Such a situation is apparent
for the ichnogenera Chaetosalpinx (Stasińska 1958, pl. 3,
fig. 2; pl. 4, figs 2–4; Klaamann 1959, pl. 4, fig. 5; Plusquellec 1968b, text-fig. 1; Oekentorp 1969, text-figs 1–2),
Helicosalpinx (Hubmann 1991, pl. 2, figs 1–3; Tapanila
2004, text-fig. 3) and Actinosalpinx (Oekentorp 1969,
text-fig. 4). Important proof of perforation was given by
Tapanila (2002, text-fig. 2), who illustrated Chaetosalpinx
ferganensis within the septa of sarcinulid tabulates. Such a
placement would be impossible without perforation of
the soft tissue. Perforation of coral tissue occurs in
modern associations between corals and other organisms
(e.g. larvae of pyrgomatid barnacles perforating the soft
tissue of recent scleractinians; Ross and Yamaguchi 2001;
Tapanila 2005).
The coral was damaged (bored) by the infesting organism (negative affect), while the settling organism benefited
from this situation, at least by having a habitat and protection by the host’s nematocysts. This situation does not
accord with the definition of commensalism. Moreover, if
Tapanila’s statement (2005) about the inhibition of
growth is true, it would strongly support my opinion on
the negative effect on the coral. Regardless, the perforation alone would have affected the attacked organism in a
negative way.
The interaction between the coral and the endobiont
was of long duration. Chaetosalpinx rex Tapanila, 2002
from the Ordovician of Anticosti Island may be used as
an example. This organism infested the tabulate coral Columnopora and was located in host’s skeleton for over
4 years (Tapanila 2002, 2005). As noted above, Combes
(2001) regarded a long duration of interaction to be a
characteristic feature of parasitism.
The placement of the infesting organism between the
walls (or within the septa) of the coral caused anatomical changes to the corallite wall around the place of
settlement of the parasite, namely thickening and deformation (Text-figs 1, 2C–D; see also Stasińska 1958, pl.
3, fig. 2; Oekentorp 1969, text-fig. 1; Tapanila 2002,
text-fig. 2). This phenomenon was recognized by
Oekentorp (1969, p. 166) as a modification of the skeletal organization of the favositids. Such modifications
prove that the infestation took place when the host was
living and that they are not post-mortem borings.
According to Combes (2001) such modifications of the
phenotype of the host are characteristic of parasitism.
Such a modification may be interpreted as Dawkins’s
(1982) ‘extended phenotype’ of the parasite. In this case
the genotype of the parasite is expressed as geometric
changes (thickening and folding) in the wall of the
host.
CONCLUSION
Perforation of the host’s skeleton and soft tissue, longterm infestations, and modification of the host’s phenotype are clear signs of parasitism. It may be supported by
possible inhibition of the host’s growth. Thus, the relationship between organisms of unknown taxonomic position belonging to the ichnogenus Chaetosalpinx Sokolov,
and possibly also to the ichnogenera Helicosalpinx Oekentorp and Actinosalpinx Sokolov, on the one hand and tabulate corals on the other can best be interpreted as
parasitic.
ZAPALSKI: PARASITISM VERSUS COMMENSALISM IN TABULATE CORALS
Acknowledgements. I express my warmest thanks to Prof. Bruno
Mistiaen (Lille), Prof. Euan N. K. Clarkson (Edinburgh) and Dr
Adam T. Halamski (Warsaw) for useful comments that
improved this paper. Drs Jarosław Stolarski (Warsaw) and Yves
Plusquellec (Brest) kindly gave me information on the relationship between the skeleton and soft tissue in modern and fossil
corals. I am also deeply grateful to Drs Ian D. Somerville (Dublin), Graham Young (Winnipeg) and an anonymous referee for
their constructive criticism and numerous comments.
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