Journal of Invertebrate Pathology 99 (2008) 254–256
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Rhabditophanes schneideri (Rhabditida) phoretic on a cave pseudoscorpion Bozˇidar P.M. C´urcˇic´ a,*, Walter Sudhaus b, Rajko N. Dimitrijevic´ a, Slobodan E. Makarov a, Vladimir T. Tomic´ a a b
Institute for Zoology, Faculty of Biology, University of Belgrade, 11000 Belgrade, Serbia Arbeitsbereich Zoologie, Institut für Biologie, Freie Universität Berlin, 14195 Berlin, Germany
a r t i c l e
i n f o
Article history: Received 24 March 2008 Accepted 23 July 2008 Available online 31 July 2008 Keywords: Rhabditids Pseudoscorpions Rhabditophanes schneideri Neobisium rajkodimitrijevici Phoresy Caves Serbia
a b s t r a c t Information of phoretic nematode-pseudoscorpion associations and cases of parasitism on five European species of pseudoscorpions was summarized by C´urc´icˇ et al. [C´urcˇic´, B.P.M., Dimitrijevic´, R.N., Makarov, S.E., Lucˇic´, L.R., C´urcˇic´, S.B., 1996. Further report on nematode–pseudoscorpion associations. Acta arachnol. 45, 43–46; C´urcˇic´, B.P.M., Sudhaus, W., Dimitrijevic´, R.N., Tomic´, V.T., C´urcˇic´, S.B., 2004. Phoresy of Rhabditophanes schneideri (Bütschli) (Rhabditida: Alloionematidae) on pseudoscorpions (Arachnida: Pseudoscorpiones). Nematology 6 (3), 313–317]. An examination of a sample of the cavernicolous pseudoscorpion Neobisium rajkodimitrijevici (C´urcˇic´ and Tomic´, 2006) (comprising a holotype male and a paratype tritonymph) from a cave in Eastern Serbia revealed this false scorpion to be a nematode carrier; the present paper reports this finding and extends our knowledge of phoresy of Rhabditophanes on pseudoscorpions. This is the first time that the rhabditid R. schneideri (Bütschli, 1873) has been noted in association with a cavernicolous pseudoscorpion. There must be some patchily distributed micro-habitats in caves where saprobiotic nematodes and small arthropods can complete their life-cycles, for example something like deposits of bat guano. The transportation of Rhabditophanes J3 by pseudoscorpions indicate that Neobisium specimens often visit these micro-habitats to find their prey. Ó 2008 Elsevier Inc. All rights reserved.
1. Introduction Since Lesne (1896) proposed the term ‘‘phorésie” (English: phoresy) to designate the transport of certain arthropods on the bodies of other arthropod species, many cases in beetles, pseudoscorpions, mites, nematodes, and some other taxa have been reported (summarized by Clausen, 1976; Matthes, 1978; Binns, 1982; Kiontke, 1997). It is notable that phoresy is perhaps the most common type of relationship observed in the fossil record by workers investigating amber (Poinar, 1992). We define phoresy as that phenomenon where an individual of a different species serves only as a means of transportation to a certain place (e.g., a new habitat with a potentially adequate supply of food such as that, stored in a brood cell, deposited egg masses, etc.). Usually the phoretic nematode has a specialized transport stage that does not feed during the time of transport. So it is not parasitic during this period, even if it might be parasitic later in its life cycle. We therefore we call the phoretic partner the carrier and avoid the term ‘‘host” used in parasitic relationships. Internal transport, for instance in the alimentary tube or within certain glands, is called endophoresy. In nematodes phoresy is common in Rhabditida living in patchily distributed habitats. Phoretic behavior is a strategy to exploit transitory habitats like dung, carcasses, or various rotting material * Corresponding author. Fax: +381 2638 500. E-mail address:
[email protected] (B.P.M. C´urcˇic´). 0022-2011/$ - see front matter Ó 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.jip.2008.07.007
that otherwise would be unavailable. In this group it is the ‘dauer’ or non-feeding third stage juvenile which is carried by arthropods (mostly Coleoptera, sometimes Diptera, Hymenoptera, and others). Not as frequent in these biochores as species of rhabditids and diplogastrids is Rhabditophanes, a group of three or four valid species, though 10 names of described species exist. Rhabditophanes aphodii (Sachs, 1950) is a rare species in cow pats which exhibits waving dauer juveniles that embark on different dung beetles for transport (Sachs, 1950). Rhabditophanes insolitus Fuchs, 1930 was found by Fuchs (1930) in frass of the curculionid Pissodes piceae and dauer juveniles on its larvae and pupae. Fuchs (1930) would have mentioned it if the dauers were affixed by their anterior end as a result of secretion and curled up like a watch-spring. This is just what was first observed by Moniez (1891) in an unidentified species and later documented by Bovien (1937) in a species from decaying vegetable matter which he assigned to R. quadrilabiatus (Cobb, 1924) and which today is regarded as identical with Rhabditophanes schneideri (Bütschli, 1873). There are only a few records of arthropods with such typically coiled third stage juveniles of R. schneideri attached to their exoskeleton. Moniez (1891) described them adequately from a mite (Gamasidae) from cow dung, where the nematodes were attached to the edge of the body, the legs and the chelicerae. Bovien (1937) found them fastened to the legs, thorax, head, etc., of staphylinid beetles and larvae from decaying vegetable matter and in experiments on the tarsal joints of the carabid Amara. Further observa-
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tions are from Collembola (Delamare Deboutteville and Théodoridès, 1951); Oribatidae (Travé, 1956); the beetle Lathridius nodifer (Lathridiidae), where dauers were fastened to the edge of the pronotum and the legs (Théodoridès, 1955); the spider Centromerus sylvaticus (Linyphiidae) (Noordam et al., 1997); and three species of pseudoscorpions mostly on the legs (C´urcˇic´ et al., 2004). On two further occasions W.S. was able to verify this association with collembolans from compost and with an oribatid mite (resembling Mesoplophora) from rotten wood. In neither case was it possible to establish cultures from these dauers for experiments on phoresy. When some tiny staphylinids were added to hundreds of coiled dauer juveniles in an agar culture of R. schneideri isolated from a slug (Deroceras reticulatum), attachment of dauer juveniles could not be observed. Information on phoretic nematode-pseudoscorpion associations and cases of parasitism.by Mermithidae on five European species of pseudoscorpions were summarized by C´urcˇic´ et al., 1996, 2004). An examination of a sample of the cavernicolous pseudoscorpion Neobisium rajkodimitrijevici (C´urcˇic´ and Tomic´, 2006) (comprising a holotype male and a paratype tritonymph) from a cave in Eastern Serbia revealed this false scorpion to be a nematode carrier, thereby bringing the total number of cases of pseudoscorpion–nematode relations to 19 (C´urcˇic´ et al., 1996). The present paper reports this finding and extends our knowledge of phoresy of Rhabditophanes on pseudoscorpions. 2. Material and methods On 13 April 1980, a holotype male and a paratype tritonymph of the cave-dwelling pseudoscorpion N. rajkodimitrijevici (C´urcˇic´ and Tomic´, 2006) were found to inhabit the Rajkova Pec´ina Cave near Majdanpek in Eastern Serbia (C´urcˇic´ and Tomic´, 2006). Both type specimens of this new taxon were dissected and mounted on slides in anhydrous glycerol medium for further study; afterwards, they were transferred to permanent slides and kept in Canada balsam. Both specimens of N. rajkodimitrijevici are deposited in the collection of the Center for Biospeleology, Institute of Zoology, University of Belgrade, 11000 Belgrade, Serbia (IZB 174–175). In their description of the new cave pseudoscorpion, C´urcˇic´ and Tomic´ (2006) noted that ‘‘rhabditid nematodes were found attached to the bodies of both the holotype male and the paratype tritonymph”. To our knowledge, this is the first report of nematode phoresy of pseudoscorpions in caves (C´urcˇic´ and Tomic´, 2006). 3. Results The rhabditid nematodes could be identified to R. schneideri (Bütschli, 1873). Only in this species are ‘dauer’ juveniles (J3) glued on arthropods with their anterior end and coiled more or less like a spiral (Fig. 1). A total of 60 attached J3 were observed on the two specimens of N. rajkodimitrijevici, 42 on the adult male and 18 on the tritonymph. It is interesting to note that many more rhabditids were attached to the adult specimen. An analysis of the sites of attachment J3 on parts of the different body (on both the left and right sides) revealed that they were abundant on the pedipalps (38%), less frequent on the four legs (legs I: 12%, legs II–IV: 15 % each), and only sporadically present (in the tritonymph) on the opisthosoma (5%), where they occupied mid-abdominal positions (Fig. 1). Phoretic rhabditids were not recorded on the prosoma and the chelicerae. The v2 test showed no significant difference in the disposition of these phoretic rhabditids between the left and the right sides of the body of the carrier. The comparison of attachment sites of R. schneideri J3 on different leg joints for the pedipalps revealed 52% on the chelae; 13%
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Fig. 1. Positions (arrows) of some Rhabditophanes rhabditids on left pedipalpal femur of the pseudoscorpion Neobisium rajkodimitrijevici.
each on the patellae, femora, and coxae; and 9% on the trochanters (Fig. 1). However, none were present on the chelal fingers. The corresponding data for legs I–IV podomeres are 18% of J3 attached on the tarsi, 20% on the metatarsi, 18% on the tibiae, 15% on the patellae, 23% on the femora (Fig. 1), 6% on the trochanters, and none on the coxae. The v2 test showed no significant difference of their disposition on the left and right podomeres. 4. Discussion It is important to note that the pseudoscorpion species studied is a cave-dweller (troglophilic). Since both adult and tritonymph stages of N. rajkodimitrijevici were found in a cave and exhibit reduced eyes and attenuated appendages, it may be assumed that its complete life cycle is restricted to an underground milieu. The nematode R. schneideri was previously reported from caves by Hnatewytsch (1929; named Rhabditis cobbi) and by Delamare Deboutteville and Théodoridès (1951; named Cheilobus quadrilabiatus). In the latter case, J3 were affixed on springtails. This is the first time that the given rhabditid has been noted in association with a cavernicolous pseudoscorpion. There must be some patchily distributed micro-habitats in the caves where saprobiotic nematodes and small arthropods can complete their life cycles, for example something like deposits of bat feces. The transportation of Rhabditophanes J3 by pseudoscorpions indicates that Neobisium specimens often visit these micro-habitats to find their prey. In comparison with our earlier study on the association of Rhabditophanes with pseudoscorpions from leaf litter, soil and humus (C´urcˇic´ et al., 2004), which showed maximum numbers of 11, 13, 26 and 35 nematodes on one pseudoscorpion (mean of 3.6 for 63 infested pseudoscorpions), the numbers of 18 and 42 J3 on one carrier are very high. This might indicate that transportation on pseudoscorpions in the cave does not occur accidentally, but that Neobisium regularly frequents a habitat which has been exhausted for the nematodes or even stayed there for a longer period. This should increase the chances for dauer juveniles to climb on a pseudoscorpion and fasten at suitable sites. In our earlier study and the present work the majority of riders (34 versus 38%) were found on the pedipalps and only a very few on the body (3 versus 5%). There is no good correspondence between the two studies in regard to the percentage of J3 on specified leg joints, except that the proximal joints are almost never chosen (none on the coxae, 3 versus
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6% of nematodes on legs attached to the trochanters). A direct observation of ascending dauer juveniles on an arthropod is necessary to find a possible interpretation of the detected pattern of attachment sites. It is clear from published data and the here presented observations that R. schneideri dauer juveniles are unspecific with respect to the carrier, affixing themselves to any arthropod with which they come into contact (springtails, mites, beetles, spiders, pseudoscorpions). Fastening by means of a secretion was a preadaptation of the nematodes enabling them to broaden the spectrum of carriers and also use those arthropods that do not offer crevices or cavities on their bodies to crawl into and find shelter. This is also the case with dauers of Pelodera cystilarva glued with their anterior end to the exoskeleton transported in that way by mites in compost (Sudhaus, 1976; Poinar, 1983). The precondition for this adhesive behavior was an altered mode of ecdysis (molting), where the J3 breaks the cuticle of the preceding stage in the caudal region and escapes with its tail tip ahead. Molting occurs after the carrier reaches a habitat favorable for further development of the nematode. It is unknown how R. schneideri leaves the J2-cuticle and what the triggers for ecdysis are. One additional point should be mentioned. Some pseudoscorpions of the Cheliferinea (Atemnidae, Cheliferidae, Chernetidae) exhibit phoresy on different insects and small mammals which transport them to bird nests, mammal nests or nests and galleries of insects (Matthes, 1978). On two occasions, we isolated R. schneideri from nests of mice in Germany. Thus, the possibility exists that nematodes attached to a pseudoscorpion might be hyperphoretically transported on a specimen that for its part is carried in the fur of a small mammal or one clinging by its pedipalp to an insect.
Acknowledgment The financial support of the Serbian Ministry of Science (Grant No. 143053) is gratefully noted.
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