Evidence of brachiopod shell infestation by tube dwelling parasitic-commensal organisms is very rare in the fossil record. The oldest record of this kind of biotic interaction is known as Eodiorygma acrotretophilla from the Early Cambrian phosphatic acrotretoid Linnarsonia. The youngest evidence of parasitic infestation was documented in the Early Cretaceous rhynchonellide Peregrinella multicarinata. Two other records of vermiform tubes inside brachiopod shells come from the Devonian. These are Diorygma atrypophilia, infesting Givetian atrypide shells, and Burrinjuckia spiriferidophilia, found in some Emsian spiriferides. Here we describe the fifth record of this kind of infestation for which a name Haplorygma dorsalis ichnogen. et ichnosp. nov. is proposed. The tubular infestation structure was revealed in two silicified dorsal valves of spirolophous brachiopods found in the Mississippian Muhua Formation of the Southern China. The affinity of the tube-dwelling organism is rather enigmatic, but its annelid relationship and kleptoparasitic nature seems highly probable. In addition, the phoronid affinity of Diorygma is here questioned.
Infestations inside brachiopod shells in the form of tubular vermiform outgrowths (bioclaustrations of Palmer and Wilson 1988; see also Tapanila 2005) are very scarce in the fossil record. One of the most remarkable skeletal responses of this kind is Diorygma atrypophilia Biernat, 1961. This endosymbiont was revealed in the interior of the ventral valves of the Middle Devonian atrypoid Atrypa zonata Schnur, 1851 (subsequently re-assigned to Desquamatia subzonata Biernat, 1964) from Poland (Biernat 1961). The second record of tubular trace fossil inside brachiopod shells was described as Burrinjuckia spiriferidophilia Chatterton, 1975. It was described in three different Emsian spiriferides from Australia by Chatterton (1975). Recently, two other cases of biotic interaction between the brachiopod host and tube-dwelling infester were recorded. One of them has been described as Eodiorygma acrotretophilia Bassett, Popov, and Holmer, 2004 from a Lower Cambrian organophosphatic lingulate brachiopod (Bassett et al. 2004). Lately, the worm-infested specimens of the Early Cretaceous hydrocarbon seep-restricted brachiopod Peregrinella multicarinata Lamarck, 1819 from southeastern Crimea, Ukraine were documented by Kiel (2008).
This paper describes a fifth and the youngest in the Palaeozoic phenomenon of such biotic interaction revealed in the Mississippian (Tournaisian) spiriferide and spiriferinide brachiopods that were equipped with the spirolophe lophophore. Thus, entire extent of time in which this particular kind of relation has been documented spans from the Early Cambrian to the early Cretaceous.
Material and methods
In studies of the Tournaisian silicified brachiopod fauna from Muhua (Guizhou Province, Southern China) conducted by the authors (e.g., Baliński 1995; Sun and Baliński 2008), two dorsal valves among several thousands of specimens preserve evidence of endosymbiotic infestation. The infested specimens include the spiriferide Tylothyris laminosa (M'Coy, 1841) and the spiriferinide Spiriferellina cf. insculpta Phillips, 1836.
A single juvenile dorsal valve of Tylothyris laminosa measuring 3.7 mm in width and 2.4 mm in length and collected from sample MH1 has a very small, simple tube growing from its inner surface (Fig. 1B). The tube is about 600 µm long and 160–190 µm thick. It has an apical, presumably single (there is some siliceous deposit obscuring the aperture), subcircular opening 90 µm in diameter. This tubular out-growth is located on the inner right flank of the valve not far from the median fold. It is posteromedianly directed, somewhat sinuous, with its tip turning ventrally. Although the ultrastructure of the tube cannot be assessed due to silicification, it is clear that it was originally secreted by the brachiopod outer mantle lobe.
A structure similar to that in T. laminosa has been found also in one dorsal valve of Spiriferellina cf. insculpta Phillips, 1836 from the sample GB (Fig. 1A). The dorsal valve, although imperfectly preserved, is about 7.8 mm wide and 5.1 mm long. The tube is located on the left internal flank of the valve in its posterior region and is posteromedianly inclined with its distal part upturned ventrally. The tube is about 750 µm long, 190–240 µm thick, with a single subcircular aperture 90 µm in diameter.
The two aforementioned specimens indicate a very low frequency of endosymbiotic infestation among brachiopods from the Muhua Formation. In the case of Tylothyris laminosa it is one out of 90 specimens whereas in Spiriferellina cf. insculpta a single infested dorsal valve was found among 6 specimens.
The tubular outgrowths described above were presumably inhabited by an unknown vermiform filter-feeding organism whose larva infested the dorsal valve of the brachiopod host either by entering its mantle cavity or by attaching directly to the anterior margin of the valve. In either case the growing body of a vermiform intruder was isolated by brachiopod mantle secreting the secondary shell material continuous with rest of the shell. The valve of Tylothyris attained at the moment of infestation probably about 1.5 mm in length and that of Spiriferellina attained about 2 mm length. In both cases the distal end of the fully grown tube extended into the mantle cavity close to the first or second turn of the spiral lophophore of the host (Fig. 2).
The general morphology of the protuberance on the inner surface of the dorsal valve of Tylothyris laminosa and Spiriferellina cf. insculpta indicates that the endosymbiotic intruder was probably an elongated, worm-like, filter-feeding small-sized organism living in the mantle cavity of the brachiopod host. The location of the tube on one side of the valve indicates that infesting organism did not intercept its food from the main inhalant feeding current of the brachiopod. Instead, it is more probable that it derived nutrition from the currents which passed through the lophophore of the host (Fig. 2).
The fossil record of parasitic—commensal infestations in brachiopod shells
The findings of tubular vermiform outgrowths inside brachiopod shells are very scarce in the fossil record. The first record of the parasitic-commensal relationship of this kind was described by Biernat (1961). She found characteristic tube-like protuberances (one or two per valve) inside as many as 15% of all ventral valves of Desquamatia subzonata Biernat, 1964 from Givetian shales in the Holy Cross Mountains, Poland (illustrated here for comparison on Fig. 1C). Each of these protuberances, named Diorygma atrypophilia Biernat, 1961, encloses two long contiguous tubes which open into the brachiopod interior by two round or slightly elliptical apertures (Biernat 1961). The outgrowths reach up to 12.2 mm in length and 2.5 mm in thickness and are anterodorsally directed. At first Biernat (1961) interpreted these structures as associated with an annelid-like parasitic organism. Later, however, McKinnon and Biernat (1970) suggested a probable phoronid relationship, pointing out that U-shaped tubes of Diorygma reflect the similarly shaped digestive tract of phoronids. This seems unlikely as phoronids are elongated worm-shaped animals having just U-shaped digestive tract, not their body (see also Emig http://paleopolis.rediris.es/Phoronida/SYST/PHORONIDA/Pho-FOSSIL/Diorygma-Eodiorygma.html). Two separate openings of Diorygma suggest that its digestive tract was straight and that its mouth and anus were located on opposite ends of a long U-turned vermiform body. This condition is unlike that in phoronids in which the gut ends close to the mouth (a result of the U-turned digestive tract) at one end of a more or less straight elongated body. It seems that the original interpretation of Biernat (1961) concerning the affinity of Diorygma is more plausible. It is not unusual to find some polychaetes housed in U-shaped galleries which have limbs running more or less straight and closely together (see, e.g., Rodrigues 2007; Rodrigues et al. 2008).
The second record of vermiform tubes inside brachiopod shells was that of Chatterton (1975). He found these structures on the inner surface of dorsal valves of three different Emsian spiriferide species from Australia and named those trace fossils as Burrinjuckia spiriferidophilia Chatterton, 1975. The tubes reach up to about 1.5 mm in diameter and are located invariably in the anteromedian part of the valve projecting sub-ventrally or anteroventrally between the bases of the spiralia. The location of the tubular protuberances indicates that they were inhabited by filter-feeding organisms that took advantage of the median inhalant feeding current of the host brachiopod (Chatterton 1975; see also Manceñido and Gourvennec 2008). According to Chatterton (1975), this is evidence of a commensal relationship between the brachiopods and Burrinjuckia spiriferidophilia (which is of uncertain taxonomic affinities).
The third recorded case of a parasitic-commensal relationship between brachiopods and tube-dwelling organisms is a unique specimen of the trace fossil Eodiorygma acrotretophilia Bassett, Popov, and Holmer, 2004 found recently in the phosphatic acrotretoid Linnarsonia constans Koneva, 1983 from the late Early Cambrian of Kazakhstan (Bassett et al. 2004). The brachiopod host is up to 3 mm in size while the tube itself is about 0.4 mm long and 0.1 mm wide with a single circular aperture 45 µm in diameter. The tube is laterally inclined indicating that the endosymbiont inhabited the brachiopod mantle cavity and exploited the host's filter-feeding system for its own respiratory and feeding needs (Bassett et al. 2004).
The fourth recorded case of a tubular infestation inside brachiopod shells was described in the Early Cretaceous hydrocarbon seep-restricted rhynchonellide Peregrinella multicarinata Lamarck, 1819 from southeastern Crimea, Ukraine (Kiel 2008). The tubes attain up to 75 mm in length and about 3.5 mm in diameter distally. They are often curved, undulating, sometimes U-turned, and always grow towards the anterior margin (= ventral margin of Kiel 2008). According to Kiel (2008) the tubes were built by polychaete worms within only the large shells of living brachiopods attaining at least 55 mm in width. A parasitic mode of life was suggested for this polychaete infester (Kiel 2008).
These four records discussed above of tubular vermiform structures inside brachiopod shells, as well as Haplorygma dorsalis ichnogen. et ichnosp. nov. reported here in the early Mississippian Tylothyris and Spiriferellina, indicate a similar phenomenon of a biotic inter-relationship (impedichnia of Tapanila 2005) between a brachiopod host and a filter-feeding organism invading its mantle cavity. However, each of these structures shows sufficient morphologic differences to distinguish them taxonomically.
The taxonomic affinity of the tube-dwelling organism inside the shell of Tylothyris laminosa (M'Coy, 1841) and Spiriferellina cf. insculpta Phillips, 1836 is very difficult to assess. Bassett et al. (2004) discussed the possible relationship of Eodiorygma with some filter-feeding organisms and their remarks may be fully applied to Haplorygma described here. They sought the probable affinity of Eodiorygma within cycliphorids (a recently described new phylum) or entoprocts. For Haplorygma an annelid affinity possibility should not be discarded as well. There are numerous reports in the literature documenting trace fossils on invertebrate skeletons which are interpreted as a result of a biotic interaction with polychaetes (e.g., Kiel 2008; Martinell and Domènech 2009). Anatomical and ecological characteristics of Haplorygma suggest that while living in the mantle cavity of a brachiopod, it nourished on stolen undigested nutrients from the host and thus probably was kleptoparasitic. While living in the shell interior of a brachiopod host an infester gained a well protected place to live and a reliable supply of nourishment.
All five records of endosymbionts in brachiopod shell have their own distinctive features and each appears isolated in space and time. Thus most probably they are not closely related to each other. On the contrary, it seems more probable that this kind of a biotic interaction between brachiopods and infesters appeared independently several times during the Palaeozoic and Mesosoic. Two of these records, namely the Cambrian Eodiorygma and Mississippian Haplorygma ichnogen. nov. are rare findings represented by one and two specimens, respectively. This suggests that relations of brachiopod host—infester in these two cases were quite unusual in those brachiopod populations, and that those infesters might have been more common in other benthic invertebrates although no evidence in the fossil record so far supports this idea. On the other hand, Burrinjuckia was found in three different species of spiriferide brachiopods and although “…only a small percentage of the total number of specimens” (Chatterton 1975: 371) were involved, several infested dorsal valves have been found. Noteworthy, Burrinjuckia shows some degree of specialisation, being invariably associated with the interior of spiriferide dorsal valves only. The case of Diorygma is distinguished by a comparatively high percentage of infested specimens. Moreover, some of the infested shells of Desquamatia subzonata show double infestation with two sub-symmetrically disposed tubular outgrowths (Biernat 1961; Fig. 1C). Diorygma is also distinguished by its apparent specialisation because it was found only in one of several other co-occurring atrypide species. What is more, in this case the infestation is associated exclusively with the ventral valves, and the tubes of Diorygma protrude into the conical spiral cavity of the infested atrypide. Thus, all five described cases of endosymbionts inside brachiopod shells have their own characteristics and peculiarities. They document what may be a wide and complex spectrum of biotic interactions that developed between brachiopods and infesters in the geological past.
Ichnogenus Haplorygma nov.
Ichnospecies type: Haplorygma dorsalis ichnosp. nov., by monotypy.
Etymology: Greek haplóos, simple, onefold, single; orygma, tunnel; from the simple tubular structure of the trace fossil.
Diagnosis.—Simple, posteromedianly inclined with distal part upturned ventrally, microscopic tubular outgrowth of the inner surface of the secondary organocalcitic shell layer of the dorsal valve of spiriferide and spiriferinide brachiopods.
Remarks.—The name of the trace fossil here described is treated in the meaning of Articles 10.3 and 42.2. of the International Code of Zoological Nomenclature (1999; see also Dzik 2005) and thus refers to the animals that are responsible for formation of the named structure. Because homeomorphy of the Cambrian Eodiorygma and Carboniferous Haplorygma is very probable (in contrary to their monophyly), we prefer to distinguish these trace fossils as separate genera.
This new genus of the trace fossils attains about 20 times smaller size of the tube than that in Diorygma Biernat, 1961 found inside shells of Desquamatia subzonata Biernat, 1964. What is more, the tube of Haplorygma is simple, inclined posteromedianly and sub-ventrally, and has only one distal aperture whereas that in Diorygma encloses two long U-turned contiguous tunnels which open distally by two round or slightly elliptical apertures and is anterodorsally inclined. The tube of the latter occurs exclusively in ventral valves of the atrypide host while the former was found in dorsal valve of Tylothyris laminosa and Spiriferellina cf. insculpta.
Haplorygma ichnogen. nov. reveals similar preference for dorsal valves of spiriferide (and spiriferinide) hosts as Burrinjuckia Chatterton, 1975 described from the Early Devonian of southern New South Wales (Chatterton 1975). The tube of the latter, however, is several times larger, shows somewhat irregular morphology, and is always located in the anteromedian part of the valve projecting sub-ventrally or anteroventrally whereas Haplorygma was found on the side of the valve and is clearly posteromedianly and sub-ventrally inclined. The polychaete tubes (not formally named) inside shells of the Cretaceous Peregrinella multicarinata Lamarck, 1819 from southeastern Crimea (Kiel 2008) are also large-sized attaining up to 75 mm in length.
In terms of size range and general appearance of the tubular outgrowth, the new genus is very similar to Eodiorygma Bassett, Popov, and Holmer, 2004 described from the late Early Cambrian of Kazakhstan (Bassett et al. 2004). Both structures do not exceed 1 mm in length. The main and obvious difference is that the structure of Eodiorygma occurs in a phosphatic-shelled brachiopod while Haplorygma is built in calcitic-shelled hosts. They differ also in the location and inclination of the tube within the dorsal valve: the Chinese form is positioned closer to the median sector of the valve whereas Eodiorygma seems more laterally located and has lateral inclination.
Stratigraphic and geographic range.—As for the type species.
Haplorygma dorsalis ichnosp. nov.
Fig. 1A, B.
Etymology: After the occurrence of the trace fossil in the dorsal valve of a brachiopod host.
Holotype: Trace fossil in the dorsal valve of spiriferide Tylothyris laminosa PKUM02-0389 figured in Fig. 1B.
Type locality: Muhua section, between villages of Muhua and Gedoungguan (Guizhou province, South China).
Type horizon: Muhua Formation, correlated with the middle Tournaisian Siphonodella crenulata Zone.
Diagnosis.—Microscopic tubular outgrowth of the dorsal valve of spiriferide and spiriferinide brachiopods, attaining 600–750 µm in length and 160–240 µm in thickness, with a single subcircular to elliptical aperture measuring about 90 µm in diameter.
Material.—One specimen of this trace fossil was found in dorsal valve of Tylothyris laminosa collected from sample MH1, the other specimen was revealed in dorsal valve of Spiriferellina cf. insculpta from sample GB.
Description.—The tubular outgrowth simple, small (see Diagnosis for detailed dimensions), posteromedianly inclined, with its distal tip upturned sub-ventrally; subcircular to elliptical in cross section.
Remarks.—As for genus.
Stratigraphic and geographic range.—Known only from the type locality, i.e., Muhua village (Guizhou Province, Southern China), Muhua Formation, Tournaisian, early Mississippian. For details on location, geology, and stratigraphy of the occurrence, see Sun and Baliński (2008).
We thank Michal Kowalewski (Virginia Polytechnic Institute and State University, USA) for offering useful comments on the first draft of the paper. The original manuscript benefited greatly from thoughtful review by the journal referee Mark A. Wilson (The College of Wooster, Wooster, Ohio, USA). This research was supported by grant from the State Committee for Scientific Research 2 P04D 021 26 (to AB).