A Devonian Spinneret: Early Evidence of Spiders and Silk Use

Reprint Series ^^fcTFNPF 27 October 1989, Volume 246, pp. 479-481 k^V/I-l-UlV/I-J

WILLIAM A. SHEAR, JACQUELINE M. PALMER, JONATHAN A. CODDINGTON, AND PATRICIA M. BONAMO

• A Devonian Spinneret: Early Evidence of Spiders and Silk Use

WILLIAM A. SHEAR, JACQUELINE M. PALMER, JONATHAN A. CODDINGTON, PATRICIA M. BONAMO

A nearly complete spider spinneret was found in Middle Devonian rocks (about 385 to 380 million years old) near Gilboa, New York. This is the earliest evidence yet discovered for silk production from opisthosomal spigots, and therefore for spiders. Two previously known Devonian fossils described as spiders lack any apomorphies of the order Araneae and are probably not spiders. The spigots of the Devonian spinneret resemble those of members of the living suborder Mesothelae, but the number of spigots and their distribution are like those of members of the suborder Opisthothelae, infraorder Mygalomorphae. The Devonian spider belonged to a clade that may be the sister group of all other spiders, of Mesothelae, or of Opisthothelae.

SPIDERS (ARTHROPODA: CHELICER- in the fossil record of spinnerets, of spiders ata: Araneae) are among the most themselves, and of silk production by ani- important terrestrial predatory animals. mals. Among the arachnids, they alone pro- Although two spider fossils have been duce silk from opisthosomal (abdominal) reported from the Devonian Period, in nei- glands that open through modified setae ther of these cases can any apomorphies of called spigots, which in turn are located on the order Araneae be demonstrated. Paleoc- reduced abdominal appendages, the spin- teniza crassipes (J), from the Lower Devoni- nerets. This character complex is the most an (404 million years old?) Rhynie Chert, is diagnostic apomorphy of spiders. We report a minute, crumpled exoskeleton that is un- here on the earliest evidence vet discovered doubtedly arachnid, but is more likely from one of the trigonotarbids that are the most W. A. Shear, Department of Biology, Hampden-Sydncy abundant animals in that deposit. Spinner- College, Hampdcn-Svdncv, VA 23943, and American ets, characteristic patterns of leg jointing, Museum of Natural History, New York, NY 10024. J. M. Palmer, Museum of Comparative Zoology, Har- eye arrangement, and other spider apomor- vard University, Cambridge, MA 02138. phies that are potentially present even in J. A. Coddington, Department of Entomology, National very small, immature animals cannot be Museum of Natural History, Smithsonian institution, Washington, DC 20560. detected in this fossil or are certainly not P. M. Bonamo, Center for Evoluoon and the Paleocnvi- there (2). Archaeometa devonica (3), from the ronment. State University of New York, Binghamton, NY 13901. slighdy later Alken-an-der-Mosel, West Ger-

27 OCTOBER 1989 REPORTS 4,79 Fig. 1. Fossil spinneret, slide 334-lb-AR34. The greatest length of the specimen (not including the Fig. 2. Distal portion of the fossil spinneret, terminal spigots) is 0.94 mm. Note the numerous showing denser clustering of spigots at tip. Mag- Fig. 4. Posterior median spinneret of Neoctemza spigots scattered along the anatomically median nification, x200. sp. (Opisthothelae: Mygalomorphae: Idiopidael. surface. Magnification, x40. The spigots are numerous, occupy the median surface, and are more densely clustered near the tip. SEM, x92. many, judging from the published photo- graphs, is not a spider and perhaps not even yet bears more than one spigot, it could not an animal fossil, rather a vertebrate copro- have come from a mesothele spider similar lite. Again, no spider apomorphies are visi- to those living today. ble on the specimen, which is simply an We have ruled out araneomorph spiders elongate blob with vague cross-striations at since the spigots of their spinnerets are one end. In our opinion, it must be rejected strongly differentiated from one another and as a possible spider fossil. from those of mygalomorph spiders in char- The earliest known terrestrial arachnids in acteristic ways (12), and all spigots on the North America occur in Middle Devonian Fig. 3. Posterior median spinnerets of Liphistius fossil specimen are of the same size and rocks near Gilboa, New York (4. 5). An malayanus (Mesothelae: Liphistiidae). Note the shape. extraordinarily diverse fauna of arthropods, single, terminal spigots, and the scalv cuticle. Mygalomorph spiders have single-articled some not yet identified, are found in this Scanning electron micrograph (SEM), x92. posterior median spinnerets with numerous Konservat Laqerstatte (a fossil deposit remark- spigots (Neoctetiiza sp.. Fig. 4) arranged as able for fine preservation, preservation of in in the fossil. The presence of undifferentiat- entire community, or both). Among recent- come from Pennsylvanian rocks, and with ed, or only slightly differentiated, spigots ly obtained specimens is a single spider two possible exceptions (8) are mesotheles, that are more densely clustered near the tip spinneret. though spinnerets are not preserved in the of the spinneret is consistent with mygalo- Recent views of spider evolution (6) di- majority and this assignment bv paleontolo- morph spider posterior median spinneret vide the order Araneae into two suborders. gists has been based on the combination of anatomy. However, both mygalomorph and Mesothelae includes a small number of spe- spider-like general morphology and a seg- araneomorph (but not mesothele) spinner- cies today restricted to southeast Asia, Indo- mented opisthosoma. Some of these fossils ets have peculiar nipple-shaped structures nesia, and Japan; they are united bv a num- are not spiders (9). A gigantic Carbonifer- called tartipores, which represent the posi- ber ot synapomorphies, including a peculiar ous arachnid from Argentina has been as- tions of spigots in previous instars (12). sense organ between the tibiae and metatarsi signed to Araneae (10) but may represent an Tartipores are not present on the Devonian of the legs (7). Mesotheles are better known unnamed order or a ricinuleid (11). In any spinneret. In addition, mygalomorph spin- for their primitive characters, including an case, this fossil, Megarachne servinei, suggests nerets usually have two types of spigots externally segmented opisthosoma and the undetected Paleozoic araneid or arachnid present. The form of the spigots themselves possession of eight (rarely seven) spinnerets, diversity. does not, in detail, agree with that of myga- which are located not at the end of the The Devonian spinneret (Figs. 1 and 2) is lomorph spigots (Table 1). opisthosoma, but near the middle of its nearly complete, consists of a single article, Mesothele spigots (Fig. 5) are uniform in ventral surface. Suborder Opisthothelae in- and carries 19 or 20 spigots that are in most morphology, with a broad, conical base and cludes all other spiders, in which the number ways characteristic of mesotheles. The spig- a long, gradually tapering, unsculptured dis- of spinnerets has been reduced to six, four, ots are arrayed along the medial surface and tal shaft that merges smoothly into the base. or two and moved to the posterior end are more densely clustered distallv. Slit sense The spigots of our fossil (Fig. 6) are of this ot the opisthosoma, which is not externally organs and setal sockets are scattered over type. segmented. Within this group, Mygalomor- the cuticle between spigots, and a few of the Mygalomorph spigots usually have an ar- phae ("tarantulas" in the North American sockets retain setae, which may be either ticulated shaft, which joins the base bv sense) have lost all vestiges of the anterior smooth or serrate. The cuticle itself has a means of a well-defined, sleevelike fold. At median spinnerets, while Araneomorphae scaly appearance, as does that of living me- least the distal third of the shaft is sculp- carry a cribellum (repeatedly lost in many sotheles. However, in mesotheles the large tured. However, the rastelloid clade of mv- lines) homologous to the anterior median lateral spinnerets of each pair are pseudoseg- galomorphs have nonarticulated shafts and spinnerets of mesotheles, and have che- mented, with spigots in ranks of two, three, extremely fine sculpture, visible only when licerae rotated to the labidognath posi- or four on the mesal surface of a pseudoseg- viewed with a scanning electron microscope. tion, so that the fangs point toward one mental ring, and the smaller, single-articled Diagenetic changes in the fossil spinneret another. median ones bear only a single spigot (Li- may have made it impossible to resolve such Aside from the Devonian examples men- phistius maylayatms, Fig. 3). Because the De- fine detail as the distal shaft sculpture of tioned above, all Paleozoic fossil spiders vonian spinneret is not pseudosegmented, Neoaeniza. Considering the absence of tarti- 4«o SCIENCE, VOL. 246 Table 1. Comparison of spinnerets. The report (21) of an archaeognath insect from the Lower Devonian (Emsian), and Liphistius the presence in the later (Givetian) Gilboa Character (mesothele) Devonian fossil Mygalomorph posterior median spinneret posterior median spinneret fauna of similar material (4) establishes an spinneret early origin for insects. Devonian material of winged (pterygote) insects may well be Spigot arrangement Single apical spigot 19-20 on mesal side Numerous on mesal side of spinneret, not of spinneret, not ranked, found in the near future. ranked, clustered clustered at tip The Devonian spider, therefore, was per- at tip haps a sit-and-wait, tunnel or tube-dwelling Spigot types One One Rarely one, usually two predator on cursorial arthropods, but mav Cuticle texture Scaly Less pronounced Slightly scaly scales just possibly have made an aerial web. Shaft sculpture Absent Apparendy absent Present on at least distal third Shaft-base union Smoothly graded Smoothly graded Collar-like articulation Tartipores Absent Absent Present REFERENCES AND NOTES 1. S. Hirst, Annu. Mao. Sal. Hist. 9. 455 (1922). 2. W. A. Shear, unpublished observations. The specimen was studied intensively using Nomarski optics; pores and the possibility that distal sculpture 35 serial optical sections were photographed, digi- tized, and reconstructed on a computer. The result- is absent, not eroded by postmortem ing image could be examined from all angles; no changes, the spigots are more like mesothele spider apomorphies were found. spigots than mygalomorph ones. 3. L. Sttfrmer, Senckenb. Lethaea 57, 121 (1976). 4. W. A. Shear et al.. Science 224. 492 (1984). As already discussed above, the combina- 5. W. Shear, P. Seldcn, W, D. I. Rolfc, P. Bonamo. J. tions of apomorphies found in spinnerets of Grierson, Am. Mus. Novit., no. 2901, 1 (1987); R. the three living clades would seem to ex- Norton, P. Bonamo, J. Grierson, W. Shear, /. Paleontol. 62, 259 (1988); W. Shear and P. Bonamo, clude the fossil from all of them. The ques- Am. Mus. Sovit., no. 2927, 1 (1988). tion then becomes placement of the Devoni- 6. N. Plamick and W. Gertsch, Am. Mas. Novit., no. 2607, 1 (1976); R. Raven, Bull. Am. Mus. Sal. an spider as a sister group of one, two, or all Hist. 182, 1 (1985). of these clades. The presentlv accepted 7. N. Platnick and P. Golobotf. J. NY Entomol. Soc. three-taxon statement for the groups of spi- Fig. 5. Terminal spigot on posterior median 93, 1265 (1985). 8. W. A. Shear, unpublished observations. Archaeometa ders so far discussed is (Mesothelae (Myga- spinneret of L. malayanus. SEM, x510. nephitina Pocock and Arachnometa luberculaia Petrun- lomorphae (Araneomorphae))). The spider kevitch [both Late Carboniferous; British Museum that bore the fossil spinneret is probably not of Natural History (BMN'H), specimens Inl5863. In31259. and Inl3914. respectively] mav be aran- a member of the sister group of either eomorphs. Araneomorphae or Mygaiomorphae, be- 9. W. A. Shear, unpublished observauons. Proaeniza brittamca. Petrunkcvitch (Late Carboniferous; cause to place it in either of those positions BMNH specimen In22834), for example, has the would require the ad hoc secondary loss of ventral opisthosomal surface very wcli preserved, tartipores in the fossil clade. Thus the fossil but shows no spinnerets. It is probably an amblypy- gid. mav be a representative of the sister group 10. M. Hiinickcn, Bol. Acad. Sad. Ciencias. Cordoba, to all other spiders, to Mesothelae, or to Argentina 53, 317(1980). Opisthothelae. Additional evidence from 11. P. Selden, personal communicaaon. 12. J. Coddington. J. Arachnol. 17, 75 (1989); J. Ko- other parts of the Gilboa spider is required voor, in Ecophystoloay of Spiders, W. Ncnrwig, Ed. to further refine its position, since all ob- (Springer-Vcrlag, New York, 1986), pp. 160-186. servable character states of the spinneret are 13. J. Schultz, Biol. Rev. 62, 89 (1987). Fig. 6. Spigot base from fossil spinneret. Oil 14. J.-C. Gall, Mem. Service Cane Geol. d'Alsace Lorraine plesiomorphic. immersion, Nomarski interference contrast op- 34, 1 (1971). However, the early appearance of every 15. K. Eskov, S. Jahrb. Geol. Palaeonlol. Monalsh. 11, tics, x 1000. 645 (1984); S. Jahrb. Geol. Palaeonlol. Abh. 175, 81 phvsical modification required to produce (1987). silk at a level of sophistication paralleling 16. P. Seldcn, personal communication; J. McAlpinc that of some modern spiders is striking. It make aerial webs but use silk only as a and I. Martin, Gin. Bttomol. 101, 827 (1969). 17. R. Raven, Bull. Am. Mus. Sat. Hist. 182, 12 (1985). relatively constant rates of evolution are burrow-and-door lining, as trip lines extend- 18. F. Coyle, in Spiders: Webs, Behavior, and Evolutton. W. assumed, it suggests a long period of pre- ing from the mouth of the burrow, and as A. Shear, Ed. (Stanford L'niv. Press, Stanford. CA, 1986), pp. 274-279, figures 10.6 and 10.7; Bull. Middle Devonian evolution for spiders and the material for egg sacs. However, when Am, Mus. Sat. Hist. 187. 205 (1988). their relatives, and that even Devonian fos- spiders make trap doors, there are specific 19. W. A. Shear, in Spiders: Webs, Behavior, and Evolution, sils will not shed much light on the origins adaptations present to shorten and broaden W. A. Shear. Ed. (Stanford Univ. Press, Stanford, CA, 1986), pp. 364-400; W. Ebcrhard, Md• pp. of spider spinning {13). While mesotheles the spinnerets (17), which are not present in 72-75; J. Coddington. ibid., pp. 326•334. may have achieved their modem form by the our specimen. Rudimentary aerial webs are 2«. R. Wootton, Annu. Rev. Entomol. 26, 320 (1981). 21. C. C Labandeira. B. S. Bcall. F. M. Hucber. Science Pennsylvanian, definitively opisthothele fos- made by a few mvgalomorphs (18), and 242,913 (1988). sils do not appear until the Mesozoic [Trias- many araneomorphs weave highly derived 22. We thank A. Robbie, who prepared the specimen, sic (14), Jurassic (15), Cretaceous (16)], and ones (19), a habit that may be correlated N. Plamick, who loaned material of Liphistius, and P. Selden, for commenting on the manusenpt, and for nearly all of these fossils can be assigned to with their well-differentiated spigots. Flying discussions with W.A.S. of fossil spiders. The com- families still extant•they are in every detail insects, against which aerial webs would ments of two anonvmous reviewers improved the (the preservation is exquisite) the equivalent have been directed,, do not appear in the manuscript. Supported bv NSF grants BSR 85-084- 42 and BSR 88-180-27 to W.A.S. and P.M.B., and of living species. fossil record until much later [Carbonifer- bv a research grant from the Power Authority of To what use Devonian spiders put their ous: Namurian (20)] but may have had a New York State to P.M.B. silk is unclear. Living mesotheles do not long history previous to that appearance. 30 June 1989; accepted 29 August 1989

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