Arthropod Structure & Development 36 (2007) 401e407www.elsevier.com/locate/asd

Comments on the eyes of tardigrades

Hartmut Greven*

Institut fur Zoomorphologie und Zellbiologie der Heinrich-Heine-Universitat Dusseldorf,

Universitatsstr. 1, D-40225 Dusseldorf, Germany

Received 3 April 2007; accepted 25 June 2007

Abstract

A survey is given on the scarce information on the visual organs (eyes or ocelli) of Tardigrada. Many Eutardigrada and some Arthrotardi-grada, namely the Echiniscidae, possess inverse pigment-cup ocelli, which are located in the outer lobe of the brain, and probably are of cerebralorigin. Occurrence of such organs in tardigrades, suggested as being eyeless, has never been checked. Depending on the species, response to light(photokinesis) is negative, positive or indifferent, and may change during the ontogeny. The tardigrade eyes of the two eutardigrades examinedup to now comprise a single pigment cup cell, one or two microvillous (rhabdomeric) sensory cells and ciliary sensory cell(s). In the eyes of theeutardigrade Milnesium tardigradum the cilia are differentiated in an outer branching segment and an inner (dendritic) segment. Because of thescarcity of information on the tardigrade eyes, their homology with the visual organs of other bilaterians is currently difficult to establish andfurther comparative studies are needed. Thus, the significance of these eyes for the evolution of arthropod visual systems is unclear yet.� 2007 Elsevier Ltd. All rights reserved.

Keywords: Inverse pigment-cup ocelli; Rhabdomeric cells; Ciliary cells; Brain

1. Introduction

Tardigrades are minute metazoans living in a wide spectrumof temporary or permanent aquatic habitats ranging from thedeep sea, the psammon of the marine and freshwater environ-ments to ‘‘terrestrial’’ habitats in soil, lichens and mosses etc.(e.g. Marcus, 1929; Greven, 1980, 2007). For a long time Tardi-grada is considered as monophyletic. Regarding their organisa-tion, tardigrades might belong to the ‘‘Articulata’’ (e.g. Marcus,1929; Nielsen, 2001). Molecular phylogenies based on the ribo-somal RNA gene sequences suggest that tardigrades are Ecdy-sozoa, and that there is a sister-group relationship betweenPanarthropoda (Tardigrada þ Onychophora þ Euarthropoda)and Cycloneuralia. Presently, tardigrades appear to be the sistergroup of Euarthropoda (e.g. Moon and Kim, 1996; Garey et al.,1996, 1999; Giribet et al., 1996; Aguinaldo et al., 1997; Garey,2001; Giribet, 2003; Mallatt et al., 2004). Among tardigrades

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doi:10.1016/j.asd.2007.06.003

the Heterotardigrada and the Eutardigrada are distinct mono-phyletic groups as revealed by morphological and moleculardata. Heterotardigrada appear to include the most basal forms(e.g., Marcus, 1929; Garey et al., 1999; Nichols et al., 2006).

Tardigrades in general appear relatively poor in distinctivetraits. This might be due to their smallness, which may be aprimary or a secondary derived feature (discussed bySchmidt-Rhaesa, 2001). Since the application of the electronmicroscopic techniques, nearly each ultrastructural detail hasbeen used for phylogenetic considerations (see Greven,1982, 2007; Dewel and Dewel, 1997; Nielsen, 2001; Kristen-sen, 2003). The eyes of tardigrades, however, did not play anysignificant role in such discussions. Dewel and Dewel (1996,p. 45) stated ‘‘a lack of any evidence that they are homologouswith integumentary compound eye’’ (see also Dewel et al.,1993).

In fact, visual organs of tardigrades have been largelyneglected so far. Currently, only a few electron micrographs ofthe eye of the two eutardigrades, Hypsibius crispae (Kristensen,1982) and Milnesium tardigradum (Dewel et al., 1993; see alsoWiederhoft and Greven, 1996), are available, which have been

402 H. Greven / Arthropod Structure & Development 36 (2007) 401e407

published in articles not primarily devoted to head sensory or-gans and putative photoreceptors, but to the biology of H. crispae(Kristensen, 1982) and the general ultrastructure of tardigrades(Dewel et al., 1993).

The present survey summarizes the few sketchy data avail-able on the structure and function of the eyes in tardigrades,presents some additional details on the eye of the eutardigradeMilnesium tardigradum (Apochela, Milnesiidae) and discussesthe significance of these eyes for the evolution of arthropodvisual systems.

2. Materials and methods

Specimens of the eutardigrades Milnesium tardigradumDoyere, 1840 (Milnesiidae, Apochela) were extracted frommosses on a wall near the University Dusseldorf and examinedin a drop of water with DIC microscopy. For transmissionelectron microscopy they were fixed either in 2.5% glutaralde-hyde in 0.1 mol/l cacodylate buffer (pH 7.2) or in 1% glutar-aldehyde plus 1% osmiumtetroxide in 0.1 mol/l cacodylatebuffer (pH 7.2), and postfixed in 2% osmiumtetroxide in thesame buffer. To facilitate penetration of the fixative, animalswere partially cut with a fine scalpel. Specimens were embed-ded in Spurr’s epoxy resin (Spurr, 1969), cut with glass knives,stained with 4% aqueous uranyl acetate followed by lead cit-rate and examined in a Zeiss transmission electron microscope(EM 9). Fixation, however, has not proved satisfactory inmany cases (see also Wiederhoft and Greven, 1999).

3. Occurrence and position of eyes

Marcus (1929) stated that most Eutardigrada and the Echi-niscoidea (Arthrotardigrada) have inverse pigmented eye-cups.The occurrence of photoreceptors in other Arthrotardigrada isdoubtful and reports concerning this matter, e.g. eyes in mem-bers of the genus Styraconyx (see Kristensen, 1977; Ramaz-zotti and Maucci, 1983) deserve confirmation. Large lipidinclusions in the brain were described in the marine arthrotar-digrades of the genus Batillipes, and delusively called ‘‘li-poid’’ eyes (Kristensen, 1978). However, it is unclear yetwhether they are associated with photoreceptors and whetherthey may act as a kind of dioptric apparatus (discussed byMarcus, 1929).

The pigmented eye-cups of tardigrades are exclusively lo-cated within the head and are closely associated with the outerdorsolateral lobe of the brain. The brain consists of several cere-bral ganglia (supraoesophageal ganglionic mass), presumablyhomologous to the protocerebrum of Euarthropoda and to be de-rived from three and a half segment. For a more detailed study ofcerebral ganglia in tardigrades see Dewel et al. (1993), Deweland Dewel (1996), Wiederhoft and Greven (1996); homologyof the brain of the heterotardigrade Echiniscus viridissimus isdiscussed in Dewel and Dewel (1996). The outer lobe of thebrain varies greatly in size and length among the eutardigradespecies. Therefore, in this taxon either ‘‘posterior’’ or ‘‘ante-rior’’ eyes can be distinguished. Eyes in Echiniscoidea are

always ‘‘anterior’’ due to the short outer lobe of the brain inthis taxon.

Pigment granules of the eye cup are black and brown (Eu-tardigrada) and red or occasionally black (Echiniscidae) andtheir amount varies in the individual eyes and pigments maybe also absent (Marcus, 1929). This is probably the case inthe ‘‘blind’’ specimens described by taxonomists (see Marcus,1929; Ramazzotti and Maucci, 1983), but the occurrence oflight sensitive structures without shading pigments was neverchecked by ultrastructural studies. The nature of the pigmentsis unknown. The red eyes of the Echiniscoidea probably con-tain carotinoids (Marcus, 1929).

4. Structure of the eye

Previous histological studies stressed the simple organisa-tion of the tardigrade eye consisting of a pigment cup that in-cludes a single ‘‘clear’’ visual cell averted from the light. Thetransmission electron micrographs, however, reveal a morecomplex structure. The following description refers to theeye of M. tardigradum.

M. tardigradum has a ‘‘posterior’’ eye (Figs. 1A,B). Theeye is composed of a single cup-like pigment cell, a probablysingle cell with microvilli and at least one ciliary cell withonly a few cilia. The pigment cell forms a cup whose innerconcave face is directed outward latero-frontally (Fig. 1C).It is filled with spherical electron dense granules measuringup to 1 mm in diameter (Figs. 1CeF and 2AeF). Within thecell, some profiles of the rough endoplasmic reticulum, mito-chondria and vesicles of different shape, size and electron den-sity are seen. A large nucleus is situated near the outer convexface of the cup.

The microvillous cell lies opposite to the cup. Microvilli,i.e. rhabdomeric protrusions with a length up to 1.3 mm extendtowards the inner face of the cup crossing an electron lucentspace that represents the optic cavity (Figs. 1D and 2AeF).The cytoplasm of the microvillous cell contains smaller vesi-cles, some profiles of the endoplasmic reticulum and mito-chondria. The nucleus of this cell is located behind thepigment cell in the most anterior portion of the outer lobe ofthe brain. Latero-frontally, the optic cavity is enclosed bythe edge of the outer lobe (Fig. 2A). Anterior to the optic cav-ity, at the outer fringes of the pigmented cup, a cilium is seen(Figs. 1D and 2A,F), which is differentiated in an inner and anouter segment. The basal part of the outer dendritic segment(ciliary shaft) is surrounded by a collar-like bulge of the innersegment (Figs. 1E,F). The outer distal part branches above theprominent primary basal body (Fig. 1F) and the branches ex-tend far into the optic cavity. Ramifications contain a variablenumber of peripheral microtubules. Centrioles and rootlets areabsent. The perikaryon of the ciliary cell is located in front ofthe pigmented cup. Whether there is only one or more ciliarycells, could not be clarified. Near the pigment cell, but clearlyseparated from it by other cells, a small nerve bundle arises(Figs. 2AeC), which probably extend to the ganglion of theposterolateral sensory field (see Wiederhoft and Greven,

403H. Greven / Arthropod Structure & Development 36 (2007) 401e407

Fig. 1. Position and ultrastructural features of the eye of Milnesium tardigradum (Eutardigrada, Apochela). Anterior third (A) and head (B). Eyes are located in the

outer lobe of the supraoesophageal mass (arrows in B). (C) Low power electron micrograph of the eye (thick arrow) embedded in the outer lobe of the brain. (D)

Pigment cup and opposed microvillous cell. Note the ciliary shaft (arrow) and its branches in the optic cavity (asterisks). (E, F) Modified cilia with an outer (double

arrow) ciliary shaft and a collar-like bulge of the inner segment (asterisk); the arrow points to a basal body. bc, body cavity; bl, basal lamella; cc, circumoeso-

phageal connectives; m, mouth tube; mv, microvilli; nu, nucleus; ol, outer lobe of the supraoesophageal mass; pg, pigment granule; ph, pharynx; s, stylet gland.

404 H. Greven / Arthropod Structure & Development 36 (2007) 401e407

Fig. 2. Selected serial sections of two series (AeC and DeF) of the eye of Milnesium tardigradum (Eutardigrada, Apochela) cut nearly in cross section. Note the

cilium (arrow), and its branches in the optic cavity (asterisk), which is adjacent to the edge of the outer lobe. ne, nerve bundle; bl basal lamella; mv, microvilli; nu,

nucleus.

405H. Greven / Arthropod Structure & Development 36 (2007) 401e407

1996). The eye and the brain are surrounded by a commonneural lamella.

Dewel et al. (1993) in their review on the microscopic ana-tomy of tardigrades present two low power electron micro-graphs of the eye of M. tardigradum. The authors emphasizethe position of the eye in the lateral lobe of the brain, near‘‘the point where processes from the posterior sensory plaques(¼posterolateral sensory field; see Wiederhoft and Greven(1999), p. 180/181) enter the neuropil’’ as well as their com-position of a cup-shaped pigmented cell and two types of re-ceptor cells, at least two ciliary and two microvillous orrhabdomeric cells. In accordance with the present data, Dewelet al. (1993) did not find a direct connection of the eye to theintegument. When comparing the brain of a heterotardigradespecies with the protocerebrum of Euarthropoda, Dewel andDewel (1996) assumed a preantennal status of the eyes andan innervation by the neuropiles of the third segment.

The organisation of the eye of Halobiotus crispae seems tobe similar to that of M. tardigradum. Kristensen (1982) men-tions one to two ciliary cells, obviously located on the fringesof the pigmented cup, a microvillous cell, a pigmented cup celland four to five ‘‘epithelial cells’’, proposing a connection withthe epidermis. He hypothesizes an epidermal origin of the eye.

Regarding the number of receptor cells, the micrographs ofthe tardigrade eyes available are insufficiently detailed. Athree-dimensional reconstruction of the entire complex isneeded.

5. Responses of tardigrades to light

Since the first description of pigmented ‘‘eye’’ spots in thehead of tardigrades, they were considered to be the main pho-toreceptors responsible for the reactions of tardigrades to light(for review of the older literature see Marcus, 1929). Observa-tions concerning this matter, however, are contradictory, as re-sponses to light might be influenced by: the experimentaldesign and the artificial conditions used, e.g., the intensity oflight, the age of the animals (some species change their reac-tions throughout their life), and even by species-specific neg-ative or positive reactions (Marcus, 1929; Baumann, 1961;Ramazzotti and Maucci, 1983; for further reading see espe-cially Beasley, 2001). To my knowledge, the ‘‘blind’’ speciesof taxonomists have not been studied in this respect yet.

Marcus (1929) described a positive response to light of theheterotardigrade Echiniscoides sigismundi, a species with pig-mented eye spots, whereas the heterotardigrade Batillipes mi-rus, in which no light sensitive structures have been detecteduntil now, behaved indifferently. From the eutardigradeswith pigmented eye spots, Dactylobiotus dispar respondednegatively, whereas Pseudobiotus megalonyx responded nega-tively to direct sunlight, but positively to diffuse light (Marcus,1929). Age dependent reactions were observed in the eutardi-grades Hypsibius convergens and Macrobiotus hufelandi.Specimens of H. convergens responded positively to lightonly before the second moult (Baumann, 1961). In M. hufe-landi, the small, i.e. young, specimens showed a statisticallysignificant negative response to light, while the larger

specimens showed neither a negative nor a positive response(Beasley, 2001). Regarding the response to light, Beasley(2001) uses the term photokinesis rather than phototaxis forthese responses, because the animals showed a non-directed,random movement, which is different from a directedmovement.

6. Discussion

The eyes of the hitherto examined eutardigrades are posi-tioned in the brain and may be termed as intracerebral photo-receptors. They very likely do not have contact to the bodywall and lack a lens. The eyes are composed of a single pig-ment-cup cell, a microvillous (¼rhabdomeric or retinula)cell, and one or two modified ciliary cells. Each ciliary cellbears a cilium having few cilia with an outer dendritic segmentgiving rise to ramification. The ciliary cells resemble variousmechano- and chemoreceptors of the epidermis in Eutardi-grada (Walz, 1978, 1979; Wiederhoft and Greven, 1999).Their small number and their modification indicate functionsother than photoreception. The optic cavity crossed by micro-villi and cilia corresponds to the ‘‘clear cell’’ described byMarcus (1929). In M. tardigradum, the eye seems to be an in-tegral part of the outer dorsolateral lobe of the brain ratherthan a herein inserted derivative of the epidermis as suggestedby Kristensen (1982) for Halobiotus crispae. Affiliation to theganglion is also indicated by the common basal lamina (neurallamella) surrounding the eye and the supraoesophageal mass.However, ontogenetic studies may solve this problem moreclearly.

Photoreceptors have been classified as microvillous(¼rhabdomeric) or ciliary with a putative diphyletic (reviewsee Eakin, 1982), monophyletic (all photoreceptors are basi-cally ciliary and cilia induce formation of photoreceptiveplasma membranes; e.g., Vanfleteren, 1982) or polyphyleticorigin (Salvini-Plawen, 1982). Pietsch and Westheide (1985)considered the ciliary type of photoreceptors as a plesiomor-phic character of Eumetazoa and suggested that the rhabdo-meric type was derived several times independently by lossof the ciliary apparatus. More recently, however, molecularand genetic data support a monophyletic origin froma proto-eye (reviewed in Gehring, 2002; Arendt, 2003). Thereare numerous examples of cerebral and non-cerebral photore-ceptors in several bilaterian assemblages, which possess a vari-able number of microvillous cells together with fullydeveloped or rudimentary ciliary cells (see literature cited above).Generally, this holds for simple inverse eyes of the ‘‘ocellus-type’’ that consist of a mass of light-sensitive membranes (la-mellae, microvilli) with and without more or less arborescentcilia e both structures either may arise from the same cell orfrom different cells e, and a crescent of pigment granules thatserves as shading device. In each lineage a very large range ofcomplexity and sophistication is observed and lens-like struc-tures appear frequently. These photoreceptors are not homolo-gous to each other and have evolved convergently. Besides theliterature cited above, examples and further readings are givenin the following articles and reviews: various taxa, Eakin

406 H. Greven / Arthropod Structure & Development 36 (2007) 401e407

(1982); nematodes, Van de Velde and Coomans (1988), anne-lids, Purschke et al. (2006), plathelminths, Sopott-Ehlers(1991).

Tardigrades possess several morphological characters thatare also shared by other taxa, notably by the cycloneuraliansand the panarthropods (for review Greven, 1980, 1982,2007; see literature cited above). Having in mind the relation-ships of Panarthropoda, the tardigrade eye as described hereinand by Dewel et al. (1993) is neither similar to the compoundeyes (considered as an autapomorphy of the Euarthropoda; seePaulus, 1979, 2000; Bitsch and Bitsch, 2005), nor to the gen-erally everse median ocelli and stemmata (although consideredas ‘‘simple’’, they are more complex organized than the tardi-grade eye; see Paulus, 1979, 2000; Bitsch and Bitsch, 2005)nor to the everse or inverse frontal eyes of crustaceans (for re-view see Elofsson, 2006), nor to the everse visual organs ofonychophorans that have an optic vesicle with a lens-likestructure (Mayer, 2006). In onychophorans, eyes are consid-ered as being rhabdomeric, because cilia observed during de-velopment and present rudimentarily in adults obviously arenot involved in the formation of photoreceptor membranes(see the discussion in Mayer, 2006). Regarding the positionof the tardigrade eye there are some similarities with accessorylateral eyes found close to the main eyes in the protocerebrumof some euarthropods, which are considered as highly ances-tral in this taxon (e.g., Jamault-Navarro, 1992; for further read-ings and discussion see Heithier and Melzer, 2005). Theseputative photoreceptive organs are composed of several cellswith rhabdomeric microvilli and some screening pigmentgranules, but lack a dioptric apparatus and ciliary cells.

In conclusion, Tardigrada show a suite of morphologicalcharacters that do suggest they lie within the arthropod (Euar-thropoda þ Onychophora) clades (e.g., Marcus, 1929; Greven,1980, 1982, 2007; Dewel and Dewel, 1997; Nielsen, 2001).Their visual organ does not belong to these features. Ratherthey could be a plesiomorphic character taken from the com-mon ancestor e.g. with Cycloneuralia or with ‘‘Articulata’’ (ifsuch a lineage exists), or this type has been convergently de-veloped in various bilaterians. Interestingly, pigment-cupeyes seem to be evolutionarily conserved in larval bilaterianeyes (see Arendt et al., 2002). In this context it should be men-tioned that speculations on the evolution of tardigrades via lar-val forms, e.g. by progenesis or more generally spoken bypaedomorphosis have a long tradition (see Kennel, 1891;Dewel and Dewel, 1997).

However, future studies may reveal a larger structural di-versity of photoreceptors in the Tardigrada with traits usablefor phylogenetic interpretations.

Acknowledgements

I thank Dipl. Biol. H. Wiederhoft and Mr. Marcel Brennerfor technical help, three anonymous referees for their con-structive critique and Dr. Steffen Harzsch and Dr. RolandMelzer for inviting me to contribute these comments to thisspecial issue of ‘‘Arthropod Structure and Development’’.

References

Aguinaldo, A.M., Tubeville, J.M., Linford, L.S., Rivera, M.C., Garey, J.R.,

Raff, R.A., Lake, J.A., 1997. Evidence for a clade of nematodes,

arthropods and other moulting animals. Nature 387, 489e493.

Arendt, D., 2003. Evolution of eyes and photoreceptor cell types. International

Journal of Developmental Biology 47, 563e571.

Arendt, D., Tessmar, K., de Campos-Baptista, M.I., Dorresteijn, A.,

Wittbrodt, J., 2002. Development of pigment-cup eyes in the polychaete

Platynereis dumerilii and evolutionary conservation of larval eyes in

Bilateria. Development 129, 1143e1154.

Baumann, H., 1961. Der Lebenslauf von Hypsibius (H.) convergens Urbano-

wicz (Tardigrada). Zoologischer Anzeiger 165, 123e128.

Beasley, C.W., 2001. Photokinesis of Macrobiotus hufelandi (Tardigrada,

Eutardigrada). Zoologischer Anzeiger 240, 233e236.

Bitsch, C., Bitsch, J., 2005. Evolution of eye structure and arthropod phylo-

geny. In: Koenemann, S. (Ed.), Crustaceans and Arthropod Relationships.

CRC Press, Taylor and Francis. Book Inc., New York, pp. 81e111.

Dewel, R.A., Dewel, W.C., 1996. The brain of Echiniscus viridissimus Peterfi,

1956 (Heterotardigrada): a key to understanding the phylogenetic position

of tardigrades and the evolution of the arthropod head. Zoological Journal

of the Linnean Society 116, 35e49.

Dewel, R.A., Dewel, W.C., 1997. The place of tardigrades in arthropod evolu-

tion. In: Fortey, R.A., Thomas, R.H. (Eds.), Arthropod Relationships. The

Systematic Association, Special Volume Series, vol. 55. Chapman and

Hall, New York, pp. 109e125.

Dewel, R.A., Nelson, D.R., Dewel, W.C., 1993. Tardigrada. In: Harrison, F.W.,

Rice, M.E. (Eds.), Onychophora, Chilopoda, and lesser Protostomata.

Microscopic Anatomy of Invertebrates, vol. 12. Wiley-Liss, New York,

pp. 143e183.

Eakin, R.M., 1982. Continuity and diversity in photoreceptors. In:

Westfall, J.A. (Ed.), Visual Cells in Evolution. Raven Press, New York,

pp. 91e105.

Elofsson, R., 2006. The frontal eyes of crustaceans. Arthropod Structure and

Development 35, 275e291.

Garey, J.R., 2001. Ecdysozoa: the relationship between Cycloneuralia and

Panarthropoda. Zoologischer Anzeiger 240, 321e330.

Garey, J.R., Krotec, M., Nelson, D.R., Brooks, J., 1996. Molecular analysis

supports a tardigrade-arthropod association. Invertebrate Biology 115,

79e88.

Garey, J.R., Nelson, D.R., Mackey, L.M., Li, J., 1999. Tardigrade phylogeny:

congruence of morphological and molecular evidence. Zoologischer

Anzeiger 238, 205e210.

Gehring, W.J., 2002. The genetic control of eye development and its implica-

tions for the evolution of the various eye-types. International Journal of

Developmental Biology 46, 65e73.

Giribet, G., 2003. Molecules, development and fossils in the study of metazoan

evolution; Articulata versus Ecdysozoa revisited. Zoology 106, 303e326.

Giribet, G., Carranza, S., Baguna, J., Riutort, M., Ribeira, C., 1996. First

molecular evidence for the existence of a tardigrada þ arthropoda clade.

Molecular Biology and Evolution 13, 76e84.

Greven, H., 1980. Die Bartierchen. Die Neue Brehm Bucherei. Bd. 537. Ziemsen

Verlag, Wittenberg Lutherstadt.

Greven, H., 1982. Homologues or analogues? A survey of some structural

patterns in Tardigrada. In: Nelson, D. (Ed.), Proceedings of the Third In-

ternational Symposium on the Tardigrada, August 3e6, 1980, Johnson

City, Tennessee, USA. East Tennessee State University Press, Johnson

City, pp. 55e76.

Greven, H., 2007. Tardigrada. In: Westheide, W., Rieger, R. (Eds.), Spezielle

Zoologie. Teil 1: Einzeller und Wirbellose Tiere (2. Auflage). Elsevier

GmbH, Munchen, pp. 456e462.

Heithier, N., Melzer, R.R., 2005. The accessory lateral eye of a diplopod,

Cylindroiulus truncorum (Silvestri, 1996) (Diplopoda: Julidae). Zoolog-

ischer Anzeiger 244, 73e78.

Jamault-Navarro, C., 1992. Sur la presence d’une structure rhabdomerique

localisee intracerebralement dans le protocerebron de Lithobius forficatus

L. (Myriapode, Chilopode). In: Meyer, E., Thaler, K., Schedl, W. (Eds.),

407H. Greven / Arthropod Structure & Development 36 (2007) 401e407

Advances in Myriapodology, Proceedings of the 8th International Con-

gress of Myriapodology. Universitatsverlag Wagner, Innsbruck, pp. 81e86.

Kennel, von J., 1891. Die Verwandtschaftsbeziehungen und die Abstammung

der Tardigraden. Sitzungsberichte der Naturforscher-Gesellschaft zu

Dorpat 1981, 504e512.

Kristensen, R.M., 1977. On the marine genus Styraconyx (Tardigrada, Hetero-

tardigrada, Halechiniscidae) with description of a new species from warm

spring on Disco Island, West Greenland. Astarte 10, 87e91.

Kristensen, R.M., 1978. Notes on marine heterotardigrades. 1. Description of

two new Batillipes species, using the electron microscope. Zoologischer

Anzeiger 200, 1e17.

Kristensen, R.M., 1982. The first record of cyclomorphosis in Tardigrada

based on a new genus and species from Arctic meiobenthos. Zeitschrift

fur zoologische Systematik und Evolutionsforschung 19, 249e270.

Kristensen, R.M., 2003. Comparative morphology: Do the ultrastructural in-

vestigations of Loricifera and Tardigrada support the clade Ecydysozoa?

In: Legakis, A., Sfenthourakis, S., Polymeni, R., Thessalou-Legaki, M.

(Eds.), The new panorama of animal evolution. Proceedings of the 18th In-

ternational Congress of Zoology. Pensoft Publishers, Sofia, pp. 467e477.

Mallatt, J., Garey, J.R., Shultz, J.W., 2004. Ecdysozoan phylogeny and Bayesian

inference: first use of nearly complete 28S and 18S rRNA gene sequences to

classify the arthropods and their kin. Molecular Phylogenetics and Evolution

31, 178e191.

Marcus, E., 1929. Tardigrada. In: Bronn, H.G. (Ed.), Klassen und Ordnungen

des Tierreichs 5, Abtlg IV, Buch 3. Akademische Verlagsgesellschaft,

Leipzig, pp. 1e808.

Mayer, G., 2006. Structure and development of onychophoran eyes: what is

the ancestral visual organ in arthropods? Arthropod Structure and Develop-

ment 35. 231e145.

Moon, S., Kim, W., 1996. Phylogenetic position of the Tardigrada based on the

18S ribosomal RNA gene sequences. Zoological Journal of the Linnean

Society 116, 61e69.

Nichols, P.B., Nelson, D.R., Garey, J.R., 2006. A family level analysis of

tardigrade phylogeny. Hydrobiologia 558, 53e60.

Nielsen, C., 2001. Animal Evolution, second ed. University Press, Oxford.

Paulus, H.F., 1979. Eye structure and the monophyly of the Arthropoda. In:

Gupta, A.P. (Ed.), Arthropod phylogeny. Van Nostrand Reinhold Company,

New York, pp. 299e383.

Paulus, H.F., 2000. Phylogeny of the Myriapoda e Crustacea-Insecta: a new

attempt using photoreceptor structure. Journal of Zoological Systematics

and Evolutionary Research 38, 189e208.

Pietsch, A., Westheide, W., 1985. Ultrastructural investigations of presumed

photoreceptors as a means of discrimination and identification of closely

related species of genus Microphthalmus (Polychaeta, Hesionida).

Zoomorphology 105, 265e276.

Purschke, G., Arendt, D., Mausen, H., Muller, M.C.M., 2006. Photoreceptor

cells and eyes in Annelida. Arthropod Structure & Development 35,

211e230.

Ramazzotti, G., Maucci, W., 1983. Il phylum Tardigrada, third ed.

Memorie dell’Istituto Italiano di Idrobiologia Dott. Marco de Marchi

41, 1e1012.

Salvini-Plawen, L.v., 1982. On the polyphyletic origin of photoreceptors. In:

Westfall, J.A. (Ed.), Visual Cells in Evolution. Raven Press, New York,

pp. 137e154.

Schmidt-Rhaesa, A., 2001. Tardigrades e are they really miniaturized dwarfs?

Zoologischer Anzeiger 240, 549e555.

Sopott-Ehlers, B., 1991. Comparative morphology of photoreceptors in free-

living plathelminths e a survey. Hydrobiologia 227, 231e239.

Spurr, A.R., 1969. A low viscosity epoxy resin embedding medium for

electron microscopy. Journal of Ultrastructure Research 26, 31e43.

Van de Velde, M.C., Coomans, A., 1988. Ultrastructure of the photoreceptor of

Diplolaimella sp. (Nematoda). Tissue and Cell 20, 421e429.

Vanfleteren, J.R., 1982. A monophyletic line of evolution? Ciliary induced

photoreceptor membranes. In: Westfall, J.A. (Ed.), Visual Cells in Evolu-

tion. Raven Press, New York, pp. 107e136.

Walz, B., 1978. Electron microscopic investigation of cephalic sense organs of

the tardigrade Macrobitus hufelandi. Zoomorphologie 89, 1e19.

Walz, B., 1979. Cephalic sense organs of Tardigrada. Current results and

problems. Prace zoologiczne Zeszyst 25, 161e168.

Wiederhoft, H., Greven, H., 1996. The cerebral ganglia of Milnesium tardigra-

dum Doyere (Apochela, Tardigrada): three dimensional reconstruction and

notes on their ultrastructure. Zoological Journal of the Linnean Society

116, 71e84.

Wiederhoft, H., Greven, H., 1999. Notes on head sensory organs of Milnesium

tardigradum Doyere, 1840 (Apochela, Eutardigrada). Zoologischer

Anzeiger 238, 338e346.