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Home , Aculepeira ceropegia, Alopecosa trabalis, Cambridgea, Cesonia, Mermithidae, Pardosa agrestis

2006. The Journal of Arachnology 34:273–278

SHORT COMMUNICATION

FIRST UNEQUIVOCAL MERMITHID–LINYPHIID (ARANEAE) PARASITE–HOST ASSOCIATION

David Penney: Earth, Atmospheric and Environmental Sciences, The University of Manchester, Manchester, M13 9PL, UK. E-mail: [email protected] Susan P. Bennett: Biological Sciences, Manchester Metropolitan University, Manchester, M1 5GD, UK.

ABSTRACT. The first description of a Mermithidae–Linyphiidae parasite–host association is presented. The is preserved exiting the abdomen of the host, which is a juvenile Tenuiphantes (Araneae, Linyphiidae), collected from the Isle of Mull, UK. An updated taxonomic list of known mer- mithid hosts is provided. The ecology of known spider hosts with regard to the direct and indirect life cycles of mermithid worms suggests that both occur in . Keywords: Aranimermis, Isle of Mull, Linyphiidae, Mermithidae, Nematoda

Nematode parasites of spiders are restricted to an updated and taxonomically correct list in Table the family Mermithidae but are not uncommon 1. Here we describe the first Mermithidae–Liny- (Poinar 1985, 1987) and were first reported almost phiidae parasite–host association and discuss the two and a half centuries ago (Roesel 1761). How- ecology of known spider hosts with regard to the ever, given the difficulty of identifying and rearing life cycles of mermithid worms. post-parasitic juvenile mermithids, they have re- This paper concerns three spider specimens, one ceived inadequate systematic treatment (Poinar with a worm in situ and two that are presumed to 1985). In addition, the complete life history is have been parasitized, but from which the worms known for only one species of these spider parasites have emerged and are lost. The specimens were col- (Poinar & Early 1990). Poinar & Welch (1981) sup- lected during May 2004, in pitfall traps containing ported the use of the Agamomermis Stiles, 50 ml of 70% alcohol, from a hazel forest in the 1903 for previously described mermithids that Tireragan Estate on the Isle of Mull, UK. The spi- could not be placed in existing taxa and that were ders belong to the linyphiid genus Tenuiphantes but considered species inquirendae. This is the case for the female with the worm in situ cannot be identi- all spider mermithids described prior to 1986 (Poin- fied to species because it is a juvenile. In the spec- ar 1987). Currently three extant species of spider imen with the mermithid, the anterior and posterior mermithid parasites are recognized: Aranimermis regions of the worm have exited the abdominal cav- aptispicula Poinar & Benton 1986, A. actereki Gu- ity just anterior to the epigastric furrow and close farov & An 1987 (spider host species unknown) to the pedicel (Fig. 1), but at least one coil can be and A. giganteus Poinar & Early 1990. In addition, observed interiorly, as a distortion beneath the ab- the fossil species Heydenius araneus Poinar 2000 dominal integument, which is devoid of white gua- (a genus restricted to Tertiary fossil nine pigmentation. The worm is pale white/cream [Poinar 2003]) has been described from a crab spi- with a diameter of 0.13 mm and an approximate der (Thomisidae) in Baltic amber. length (assuming only one coil exists in the spider) Poinar (1985, 1987) provided lists of spider spe- of 15.6 mm. The body length of the spider is 2.14 cies with records of mermithid nematode parasit- mm. The two other specimens are both female Ten- ism. However, many of these taxa have now re- uiphantes tenebricola (Wider 1834) but no worms ceived taxonomic revisions and or transfers. In are visible, although the abdomens of both are se- addition, a number of subsequent reports of para- verely damaged at the same point at which the sitism have been published (Gafurov & An 1987; worm is emerging in the other specimen. We con- Poinar & Early 1990; Camino & de-Villalobos sider it probable that both of these specimens were 1998; Matsuda 1999; Poinar 2000; Allard & Rob- parasitized as well. One of the specimens has an ertson 2003; Iida & Hasegawa 2003; Vandergast & emaciated, disk-shaped abdomen (similar to that of Roderick 2003; Ahtiainen et al. 2004). We provide the specimen with the worm in situ), which gives

273 274 THE JOURNAL OF ARACHNOLOGY

Table 1.—Spider hosts of mermithid worms: * A. aptispicula,**A. giganteus, remainder species in- quirendae.

Family Species Reference Comments Agelenopsis oregonensis Cham- in Poinar (1987) berlin & Ivie 1935 Amaurobiidae Eurocoelotes inermis (L. Koch in Poinar (1987) as Coelotes i. 1855) Antrodiaetidae Atypoides riversi O.P.-Cambridge in Poinar (1987) 1833 Anyphaenidae Wulfila albens (Hentz, 1847)* in Poinar (1987) as W. alba Araneidae (Walckenaer in Poinar (1987) as Araneus ceropegius 1802) Araneidae Araneus diadematus Clerck 1757 in Poinar (1987) Araneidae Verrucosa arenata (Walckenaer in Poinar (1987) 1842)* Ctenidae Leptoctenus byrrhus Simon 1888 Poinar (2000) as Ctenus bryrrbus Cybaeidae Argyroneta aquatica (Clerck in Poinar (1987) 1757) Gnaphosidae (Hentz 1847)* in Poinar (1987) Gnaphosidae Gnaphosa lucifuga (Walckenaer in Poinar (1987) 1802) Hexathelidae Porrhothele antipodiana (Wal- Poinar & Early as P. a. (Dipluridae) ckenaer 1837)** (1990) Idiopidae Misgolas borealis (Forster Poinar & Early as Cantuaria b. (Cteni- 1968)** (1990) zidae) Linyphiidae? Micryphantes bicuspidatus C.L. in Poinar (1987) nomen dubium (Plat- Koch 1838 nick 2004) Lycosidae inquilina (Clerck 1757) in Poinar (1987) as Tarentula i. Lycosidae Alopecosa trabalis (Clerck 1757) in Poinar (1987) as Lycosa vorax Lycosidae Arctosa alpigena (Doleschall Poinar (2000) possible mermithid 1852) Lycosidae Geolycosa patellonigra Wallace in Poinar (1987) 1942 Lycosidae Hygrolycosa rubrofasciata (Ohlert Ahtiainen et al. 1865) (2004) Lycosidae agrestis (Westring 1861) in Poinar (1987) Lycosidae Pardosa amentata (Clerck 1757) in Poinar (1987) as Lycosa saccata Lycosidae Pardosa furcifera (Thorell 1875) in Poinar (1987) Lycosidae Pardosa glacialis (Thorell 1872) in Poinar (1987) Lycosidae Pardosa hortensis (Thorell 1872) in Poinar (1987) Lycosidae Pardosa lugubris (Walckenaer in Poinar (1987) 1802) Lycosidae (Hentz 1844) in Poinar (1987) as P. nigropalpis and P. scita Lycosidae Pardosa palustris (Linneaus 1758) in Poinar (1987) as Lycosa tarsalis Lycosidae Pardosa pseudoannulata (Boesen- Iida & Hasegawa berg & Strand 1906) (2003) Lycosidae Pardosa riparia (C.L. Koch 1833) in Poinar (1987) Lycosidae Pardosa sphagnicola (Dahl 1908) in Poinar (1987) as Lycosa riparia s. Lycosidae Pardosa suwai Tanaka 1985 Matsuda (1999) Lycosidae Pardosa vancouveri Emerton in Poinar (1987) 1917 Lycosidae Rabidosa rabida (Walckenaer in Poinar (1987) as Lycosa scutulata 1837) Lycosidae Schizocosa saltatrix (Hentz 1844) in Poinar (1987) as Lycosa versimilis Lycosidae Sosippus floridanus Simon 1898 in Poinar (1987) Nemesiidae Stanwellia kaituna (Forster Poinar & Early as Aparua k. (Dipluri- 1968)** (1990) dae) PENNEY & BENNETT—MERMITHID–LINYPHIID PARASITE–HOST 275

Table 1.—Continued.

Family Species Reference Comments Oxyopidae Oxyopes sertatus L. Koch 1877 Okochi (1969) Oxyopidae Peucetia viridans (Hentz 1832) in Poinar (1987) oblongus (Walckenaer in Poinar (1987) 1802) Salticidae Habronattus signatus (Banks Vandergast & 1900) Roderick (2003) Salticidae Myrmarachne formicaria (De in Poinar (1987) as Salticus formicarius Geer 1778) Salticidae Phidippus borealis Banks 1895 in Poinar (1987) Salticidae Keyserling 1885 in Poinar (1987) Salticidae Phidippus johnsoni (Peckham & in Poinar (1987) Peckham 1883) Salticidae Phidippus putnami (Peckham & in Poinar (1987) Peckham 1883) Salticidae Sitticus floricola palustris (Peck- in Poinar (1987) as Sitticus p. ham & Peckham 1883) Cambridgea foliata (L. Koch in Poinar (1987) 1872) Tetragnathidae Tetragnatha anuenue Gillespie Vandergast & 2002 Roderick (2003) Tetragnathidae Tetragnatha brevignatha Gillespie Vandergast & 1991 Roderick (2003) Tetragnathidae Tetragnatha praedonia L. Koch Okochi (1969) 1878 Tetragnathidae Tetragnatha quasimodo Gillespie Vandergast & 1991 Roderick (2003) Theridiidae Enoplognatha ovata (Clerck 1757) in Poinar (1987) as Theridion ovatum and T. redimitum Thomisidae Diaea dorsata (Fabricius 1777) in Poinar (1987) Thomisidae Misumenops tricuspidatus (Fabri- Okochi (1969) cius 1775) Thomisidae Xysticus deichmanni Soerensen in Poinar (1987) 1898 Thomisidae Xysticus durus (Soerensen 1898) in Poinar (1987) Thomisidae Xysticus funestus Keyserling 1880 in Poinar (1987) Zoridae Zora maculosa Roewer 1951 in Poinar (1987) as Z. maculata O.P.-C; nomen dubium (Plat- nick 2005)

the impression of having been host to a worm. It whereas only one female of each of the following has a normal degree of guanine pigmentation. The species was collected: T. alacris (Blackwall 1853), second specimen is not emaciated and has almost T. cristatus (Menge 1866) and T. mengei (Kulczyn- no guanine pigmentation. It cannot be ruled out that ski 1882). the specimens were damaged upon sorting the pit- Poinar (1985, 1987) cited von Siebold (1848) as fall trap contents, but as no other spiders (including having identified an unknown mermithid worm in many smaller species) were damaged, we consider the spider Micryphantes bicuspidatus (listed in Ta- this unlikely. Alternatively, they may have been ble 1 under Linyphiidae?). At the time of von Sie- hosts to non-mermithid parasites, such as acrocerids bold’s paper (his description consisted of only five or phorids. Unfortunately, the pitfall contents are no lines and no figures), only six spider families had longer available to check for emerged worms. It is been established, Linyphiidae was not erected until probable that the specimen with the worm also be- 1859. The genus Micryphantes C.L. Koch 1833 and longs to T. tenebricola, given that six other indi- M. bicuspidatus are both nomina dubia (Platnick viduals (three males and three females) were also 2005). Therefore, the new specimen described here collected at the same time from the same locality, represents the first described record of a mermithid– 276 THE JOURNAL OF ARACHNOLOGY

Figure 1.—The mermithid-carrying spider. Note the absence of abdominal guanine pigmentation, arrows point to the internal coil of the worm visible as a distortion in the integument. Scale lines ϭ 1.0 mm. linyphiid parasite–host association. Furthermore, abolic waste products for pigmentation purposes. the claims of Allard & Robertson (2003) of having Further research would be required to confirm this identified mermithids in Pardosa milvina (Hentz) hypothesis. (Lycosidae) for the first time are unjustified, be- At the time of emergence from the spider host, cause they were previously reported by Montgom- mermithid worms are mature third stage postpar- ery (1903) under the junior synonyms Pardosa ni- asitic juveniles. Thus, the individual described gropalpis Emerton 1885 and Pardosa scita above cannot be identified to species because di- Montgomery 1902. agnosis is based on adult characters. Mermithid life Being host to the worm carries a physiological cycles are either direct or indirect. Direct life cycles cost for the spider in addition to its ultimate demise are characterized by direct penetration of the spider upon the emergence of the parasite. Infection signs host through the integument by the infective stage generally start with a reduction or absence of di- larva following emergence from the . Indirect gestive structures, and other organs may also be re- life cycles involve a paratenic host (or a host in duced in extreme cases (Poinar 1985). It is inter- which significant development does not occur) in esting to note the reduced amount of guanine addition to the developmental (spider) host, which deposition in two of the above specimens, and in- is infected by ingesting the infective stage of the deed the total absence of it in the specimen with parasite (Poinar 1985). The direct cycle is by far the worm. Guanine is a crystalline purine excretory the most common among mermithids studied to product, which accumulates in specialized, periph- date, however, it has been suggested that spider eral cells of the digestive diverticula lying directly mermithids first undergo an indirect life cycle in- beneath the hypodermis (Oxford & Gillespie 1998) volving an aquatic paratenic host (Poinar 1987). and has a white, blocky appearance. Although pat- Reasoning for this was based on observations of the terns of guanine deposition can vary intraspecifi- life cycle of the spider mermithid Aranimermis ap- cally and throughout an individuals’ development tispicula as follows: ‘‘adults were found in an (Oxford 1998), there is usually a distinct pattern of aquatic , whereas parasitized spiders were guanine pigmentation present in Tenuiphantes Saar- found in a variety of . Parasitized isto & Tanasevitch 1996 specimens (DP pers. obs). spiders were observed to enter the water and the In the case of mermithid-carrying individuals how- nematodes were seen to emerge from the hosts’ ever, the worm may be compromising the spider to bodies. These observations support an indirect type such an extent, that the spider is receiving insuffi- of cycle, but further studies are required to substan- cient nourishment to produce enough of these met- tiate this’’ (Poinar 1987). Poinar (1987) did not rule PENNEY & BENNETT—MERMITHID–LINYPHIID PARASITE–HOST 277 out that some spider mermithid species may also (Museum fu¨r Naturkunde, Berlin) for providing old have a direct life cycle. The life cycle of A. actereki German literature and D. Logunov (Manchester presumably has an indirect life cycle because all Museum) for translating a Russian paper. DP ac- worms studied (12 males, two females and four knowledges a Leverhulme Trust grant to P. Selden post-parasitic larvae) were collected from the bot- and SB thanks L. Lace (Manchester Metropolitan tom of a freshwater spring (Gufarov & An 1987). University) for assistance and advice. A. giganteus from New Zealand does have an in- direct life cycle involving aquatic invertebrates LITERATURE CITED (Poinar & Early 1990). Ahtiainen, J.J., R.V. Alatalo, R. Kortet & M.J. Ran- Given that most aquatic larvae have tala. 2004. Sexual advertisement and immune winged adults, the ecology of the spider hosts may function in species (Lycosidae). Behav- provide insights that support or refute Poinar’s idea ioural Ecology 15:602–606. regarding the indirect life cycle of A. aptispicula. Allard, C. & M.W. Robertson. 2003. Nematode and For example, winged, flying are more likely dipteran endoparasites of the Par- to be consumed by web spinning or foliage/flower dosa milvina (Araneae, Lycosidae). Journal of spiders than they are by non-web spinning, Arachnology 31:139–141. ground hunters or burrowing, sit and wait predators, Camino, N.B. & L.C. de Villalobos. 1998. First oc- which can be expected to feed primarily on non- currence of a mermithid (Nematoda: Mermithi- flying, mainly fully terrestrial prey and are thus, dae) parasitizing a spider (Arachnida: Araneida) more likely to be hosts to mermithids with a direct in Argentina. Revista de la Sociedad Entomolo- life cycle. Interestingly, the ecology of all but one gica Argentina 57:6. of the spiders reported by Poinar & Benton (1986) Gafurov, A.K. & P.N. An. 1987. A new species of as hosts of A. aptispicula (Gnaphosidae, Cesonia mermithid Aranimermis actereki sp. n. (Mermi- bilineata; Thomisidae, Misumenops sp. and Tmarus thidae, Nematoda) from the Kirghizia. Izvestiya sp.; Salticidae, Phidippus sp.; Araneidae, Verrucosa Akademii Nauk Kirgizskoi SSR Khimiko Tekhn- arenata; Amaurobiidae, Wadotes sp. and Any- ologicheskie Biologicheskie Nauki 1987:79–82. phaenidae, Wulfila albens), supports the idea of an [In Russian]. indirect life cycle for this parasitic worm. The po- Iida, H. & H. Hasegawa. 2003. First record of a tential problem species of those listed is C. bilinea- mermithid nematode emerging from the wolf ta (Gnaphosidae). These are fast moving, agile spider Pardosa pseudoannulata (Araneae: Ly- hunters usually found under loose leaf litter at cosidae). Acta Arachnologica 52:77–78. ground level and males are often found in pitfall Matsuda, M. 1999. Two intersexual spiders of the traps. However, they have been collected by sweep- family Lycosidae from Japan. Bulletin of the Hi- ing low vegetation and have also been collected gashi Taisetsu Museum of Natural History 21:5– from malaise traps (Platnick & Shadab 1980), 54. [In Japanese]. which are primarily designed for catching flying in- Montgomery, T.H. 1903. Studies on the habits of sects. spiders, particularly those of the mating period. The large number of non-web spinning, cursorial Proceedings of the Academy of Natural Sciences Lycosidae (Table 1; 38% of all species, excluding of Philadelphia 55:80–90. nomina dubia) with undescribed mermithids, sug- Okochi, T. 1969. Reports on parasites of spiders. gests that a direct life cycle may be involved in Kishidaia 9:2–. [In Japanese]. some instances. Admittedly, some lycosids are Oxford, G.S. 1998. Guanine as a colorant in spi- common by freshwater, such as Hygrolycosa rub- ders: development, genetics, phylogenetics and rofasciata and Pardosa pseudoannulata (known to ecology. Pp. 121–131. In Proceedings of the 17th be mermithid hosts, see Table 1) and may be hosts European Colloquium of Arachnology, Edin- to worms with indirect life cycles. However, lycosid burgh, 1997. (P.A. Selden, ed.). British Arach- genera such as Pirata and the pisaurid genus Do- nological Society, Bucks. lomedes, which are encountered almost exclusively Oxford, G.S. & R.G. Gillespie. 1998. Evolution and near freshwater are unknown as mermithid hosts. ecology of spider coloration. Annual Review of The mermithid life cycle type in relation to the spi- Entomology 43:619–643. der host Argyroneta aquatica also poses interesting Platnick, N.I. 2005. The world spider catalog, ver- questions, as this spider spends its entire life under sion 5.5. American Museum of Natural History, water. Clearly, much work needs to be done before online at http://research.amnh.org/entomology/ we can fully understand these interesting host–par- spiders/catalog/INTRO1.html. asite relationships, but a knowledge of the ecology Platnick, N.I. & M.U. Shadab. 1980. A revision of of the host spiders can provide helpful clues in re- the spider genus Cesonia (Araneae, Gnaphosi- solving these. dae). Bulletin of the American Museum of Nat- We thank G.O. Poinar Jr. (Oregon State Univer- ural History. 165:335–386. sity) for his comments on the manuscript, J. Dunlop Poinar, G.O. Jr. 1985. Mermithid (Nematoda) par- 278 THE JOURNAL OF ARACHNOLOGY

asites of spiders and harvestmen. Journal of Ar- asite of New Zealand mygalomorph spiders (Ar- achnology 13:121–128. aneae: Arachnida). Revue de Ne´matologie 13: Poinar, G.O. Jr. 1987. Nematode parasites of spi- 403–410. ders. Pp. 299–308. In Ecophysiology of Spiders. Poinar, G.O. Jr. & H.E. Welch. 1981. Parasites of (W. Nentwig, ed.). Springer Verlag, Heidelberg. invertebrates in the terrestrial environment. Pp. Poinar, G.O. Jr. 2000. Heydenius araneus n. sp. 947–954. In Review of Advances in Parasitolo- (Nematoda: Mermithidae), a parasite of a fossil gy. (W. Slusarski, ed.). Polish Scientific Publi- spider, with an examination of helminths from cations, Warsaw. extant spiders (Arachnida: Araneae). Invertebrate Roesel, A.J. 1761. Insectenbelustigung. Johann Jo- Biology 119:388–393. seph Fleishmann, Nu¨rnberg. Poinar, G.O. Jr. 2003. Trends in the evolution of Vandergast, A.G. & G.K. Roderick. 2003. Mermi- insect by nematodes as inferred from thid parasitism of Hawaiian Tetragnatha spiders fossil evidence. Journal of Nematology 35:129– in a fragmented landscape. Journal of Inverte- 132. brate Pathology 84:128–136. Poinar, G.O. Jr. & C.L.B. Benton Jr. 1986. Arani- von Siebold, C.T.E. 1848. Ueber die Fadenwurmer mermis aptispicula n.g., n.sp. (Mermithidae: der Insekten. Entomologische Zeitung 9:290– Nematoda), a parasite of spiders. Systematic Par- 300. asitology 8:33–38. Poinar, G.O. Jr. & J.W. Early. 1990. Aranimermis Manuscript received 16 November 2004, revised 21 giganteus n. sp. (Mermithidae: Nematoda), a par- April 2005.