NORTH-WESTERN JOURNAL OF ZOOLOGY 10 (1): 133-137 ©NwjZ, Oradea, Romania, 2014 Article No.: 131305 http://biozoojournals.ro/nwjz/index.html
Silk-producing organs of the troglobitic spider species Rhode aspinifera (Nicolic, 1963) (Araneae: Dysderidae)
Jaromír HAJER, Michaela CZERNEKOVÁ and Dana ŘEHÁKOVÁ
Department of Biology, Faculty of Science, J.E. Purkinje University in Ústí nad Labem, České mládeže 8, 400 96 Ústí nad Labem, Czech Republic. E-mail’s: [email protected], [email protected] *Corresponding author, J. Hajer, Phone: +420-475-283-614, E-mail: [email protected]
Received: 4. June 2013 / Accepted: 21. September 2013 / Available online: 27. December 2013 / Printed: June 2014
Abstract. The external morphology of the spinning apparatus of the troglobitic spider species Rhode aspinifera (Nicolic, 1963) was studied using scanning electron microscopy. Three pairs of spinnerets in adult stages of both sexes are equipped with three kinds of spigots (i.e. external outlets of silk spinning glands). The silk- producing organ is equipped with the same types of glands (Glandulae ampullaceae, Gl. piriformes and Gl. psudaciniformes) as those of other dysderids studied so far; however, the total number of their spigots (and the glands connected to them) is very small. This may be an adaptive response to reduce the production of energetically costly silk.
Key words: Dysderoidea, troglobiomorphism, silk production.
Introduction of glands: the largest Glandulae ampullaceae and two considerably smaller Glandulae piriformes, The spider species Rhode aspinifera (Nicolic, 1963) which supply the anterior lateral spinnerets, and lives underground, in the karst cave system near Glandulae pseudaciniformes, which supply the pos- Postojna, Slovenia, where is usually found under terior median spinnerets and posterior lateral stones. This species has never been found outside spinnerets. The presence of only three kinds of Slovenia (Platnick 2013). The Postojna-Planina sys- spinning glands/spigots has subsequently been tem is the type locality of a number of ‘first cave confirmed in about fifty other species of the genus animals’, including the first described troglobite, Dysdera Latreille, 1804 (Arnedo et al. 1996, 2000; the beetle Leptodirus hochenwarti and the European Arnedo & Ribera 1997, 1999) and in Harpactea rubi- cave salamander Proteus anguinus (Culver & Sket cunda (C. L. Koch, 1838) (Hajer et al. 2013). The 2000). Karsts are “arks” of biodiversity and often above-mentioned genera, Dysdera and Harpactea, contain high levels of endemism (Figueras et al. represent two of the three subfamilies (Dysderi- 2013). nae, Harpacteinae and Rhodinae) of the family The biology of R. aspinifera has been described by Dysderidae, which consists of 24 genera and 526 Deeleman-Reinhold (1978) and Thaler (1990). Red- species (Platnick 2013). No SEM study of spinner- brown adult specimens with completely reduced ets or spinneret spigot morphology has been car- eyes (Fig. 1 A-B) have an opisthosoma equipped ried out for any species belonging to the third sub- with dorsal and ventral scuta and they reach a family – Rhodinae. body length of 3.3 mm and 3.8 mm respectively Based on their work on Canarian Dysdera, for males and females (Thaler 1990). Arnedo et al. (2007) concluded that spigots seem The silk spinning apparatus of spiders (Ara- to be reduced in cave-dwelling dysderids. The au- neae) consists of spinnerets and silk spinning thors suggest that such reduction may be an adap- glands located in the opisthosoma. True spiders tive response to reduce the production of energeti- (infraorder Araneomorphae with the largest num- cally costly silk. We anticipated that research into ber of species) possess three pairs of spinnerets, the silk-producing organs of Rhode aspinifera namely the anterior lateral, posterior median and would yield results that might be used to corrobo- posterior lateral spinnerets. Silk spinning glands rate this hypothesis. supply sets of jet-like spigots. The spinning appa- Therefore, the present study aims to: (1) inves- ratus of Dysderidae, including the histochemical tigate the morphology of the spinnerets, in par- characteristics of their spinning glands, has been ticular their spinning fields and spigots for described by Glatz (1972), who found that adult R.aspinifera, (2) to compare the silk producing or- females and males of Dysdera erythrina (Walcke- gans of R. aspinifera with those of other dysderids naer, 1082) were equipped with only three types investigated so far, in order to establish whether 134 J. Hajer et al.
Figure 1 A-B. Rhode aspinifera, adult female. – A. Dorsal view of the entire body; box defines area of image B. – B. Anterior part prosoma with totally reduced eyes. Abbreviations: PS = prosoma; DSO = dorsal scutum of opist- hosoma; CH= chelicerae.
and to what extent underground life results in the reduction of silk-producing organs.
Materials and Methods
All the Rhode aspinifera material studied (11 adult females and 6 adult males) came from the collection of Dr. Milan Řezáč of the Crop Research Institute in Prague, Czech Republic. The spiders were caught in August 2011 under stones in the Osojica cave, which is a part of the karst cave system near Postojna, Slovenia. The material in this collection was fixed by 80% ethanol. For scanning elec- tron microscopy studies, the spiders were dehydrated in ethanol and critical-point dried with carbon dioxide. Af- ter sputtering with gold, they were observed with a XL 30 ESEM Environmental Scanning Electron Microscope (Fig. 1B), and a TESCAN SEM (Figs. 2A-5B). Figure 1 was ob- tained using an Infinity Lite digital microscope camera Figure 2. Spinning apparatus of adult female. Arrange- connected to a NOVEX RZT-PL stereo microscope. ment of the three pairs of spinnerets; their segments are Voucher specimens were deposited at the Department of marked I.- III. Abbreviations: ALS = anterior lateral Biology, Faculty of Science, J.E. Purkinje University in spinnerets; PMS = posterior median spinnerets; Ústí nad Labem, Czech Republic. PLS = posterior lateral spinnerets.
Results spigot and three smaller piriform gland spigots (Fig. 3A), is located at the top of the apical seg- The spinning apparatus of Rhode aspinifera consists ment of each anterior lateral spinneret (Fig. 3 A-B). of three pairs of spinnerets located at the end of No differences were found in the number of spig- the ventral side of the opisthosoma (Fig. 2). Ante- ots between females and males. The ampullate rior lateral spinnerets are three-segmental. Of the gland spigots, located on the inner margin of the three segments, the second, cylindrical in shape, is spinning field, have a longer and thicker terminal the largest, whereas the basal segment is low and part, i.e. the “shaft” (Foelix 2011), in comparison easy to miss during observation. The cuticle of all with the piriform gland spigots. The basal part of the three segments bears setae, which correspond these spigots consists of a socket 8-10 µm high and to tactile hairs in their appearance. 10-12 µm in diameter. Sockets of the smaller piri- A spinning field (i.e. an area equipped with form gland spigots are only 2 µm high and 5 µm in spigots), containing a single ampullate gland diameter. Shafts of the ampullate gland spigots Spinning organs of Rhode aspinifera 135
Figure 4 A-B. Posterior median spinnerets. – A. Overall view of a pair of monosegmental spinnerets. – B. Detailed view of terminal part of spinneret. Abbreviations: PMS = posterior median spinnerets; PA bas = pseudaciniform gland spigot (basal part); PA term = pseudaciniform
gland spigot (terminal part); HA = hairs. Small arrows Figure 3 A-B. Anterior lateral spinnerets. – A. Spigot indicate tubercles on the surface of the cuticle. placement in spinning field of apical segment (III.) of ALS. – B. Detailed view of spigots. Abbreviations: AM bas = ampullate gland spigot (basal part); AM term = lateral spinnerets, posterior median spinnerets are ampullate gland spigot (terminal part); PI = piriform covered with very little hair. When compared with gland spigots; HA = hairs. Ampullate gland spigots have a partially (A) or completely (B) broken off termi- other pairs of spinnerets, the cuticle of posterior nal part (“shaft”). median spinnerets has a completely different sur- face structure, since it is dotted with tiny tubercles of unknown function (Fig. 4B). reach a length of approx. 25 µm. As the spiders Posterior lateral spinnerets are made up of were handled in the process of preparing samples two segments (Fig. 5A-B). Their basal segments, for scanning electron microscopy, shafts of ampul- cylindrical in shape, face away from the longitu- late gland spigots often broke off from the sockets dinal axis of the body at an angle. On the other (Fig. 3B). This did not occur in the case of other hand, the apical segments of the same pair face the types of spigots. centre of the opisthosoma (Fig. 5A) and are Posterior median spinnerets are one- equipped, both in males and females, with two segmented and the smallest of the three pairs of pseudaciniform gland spigots that have a low sep- spinnerets (Fig. 4A-B). The spinning field at the tum between them. There are no morphological top of each PMS both in males and females was differences between the spigots of posterior lateral equipped with two pseudaciniform gland spigots and posterior median spinnerets. with long, thin shafts (Fig. 4A). Unlike anterior The sockets of pseudaciniform gland spigots 136 J. Hajer et al.
metabolic rate (Hadley et al. 1981), a reduction in circadian rhythm (Howarth 1983), a tendency to lay a smaller number of larger eggs (Vandel 1965), and a reduction of the tracheal system (Kuntner et al. 1999, Miller 2005). Based on the study of endemic Dysdera species in the Canary Islands, which included several cases of obligate cave-dwelling species, Arnedo and collaborators (Arnedo et al. 1996, 2000; Arnedo & Ribera 1997, 1999) observed that spigots seemed to be reduced in cave-dwelling dysderids, which led him to hypothesize that this may be an adaptive response to reduce the production of en- ergetically costly silk (Arnedo et al. 2007). The small number of spigots found in Rhode aspinifera seems to support this hypothesis. The silk-producing organs, spinning activity and ways of using the silk by spiders of the genus Rhode or by any other genus of the subfamily Rhodinae have not been studied or described to date, which precludes direct comparison of the spinneret spigot morphology in R. aspinifera with any of the epigean species of a similar size belong- ing to the same subfamily. Therefore, that the re- duction of the spinning apparatus in R. aspinifera is the result of cave adaptation and not a diagnostic
feature of the genus Rhode, remains to be demon- Figure 5 A-B. Posterior lateral spinneret. – A. Detailed strated. Like other dysderids, R. aspinifera possess view of apical segment with two spigots separated by a three types of glands (ampullate, piriform and septum. – B. Detailed view of pseudaciniform gland of spigot. Abbreviations: PA bas = pseudaciniform gland pseudaciniform), but the actual numbers of glands spigot (basal part); PA term = pseudaciniform gland are small in comparison with the genera Harpactea spigot (terminal part); SP = septum. and Dysdera (see Glatz 1972; Arnedo et al. 1996, 2000, Arnedo & Ribera 1997, 1999, Hajer et al. 2013). R. aspinifera shows the smallest number of (Fig. 5B) of posterior lateral and posterior median spigots found in any dysderid studied so far. The spinnerets are approx. 5 µm high and 15-20 µm in presence of spigots of ampullate and piriform diameter. The shafts, which reach up to 50-55 µm, glands indicates that R. aspinifera has the ability to broaden out in a bulbiform fashion at the point of make draglines and attach them to the substratum connection with the sockets, so that there is hardly using attachment discs. In spiders of the infraor- any gap between the edge of the socket and the der Araneomorphae, dragline silk is produced by broader part of the shaft. This connection is a pair of ampullate glands while the material of at- probably very firm, and these shafts have not been tachment discs is secreted from piriform glands observed to break off from the sockets, unlike (Foelix 2011). Anchored to the substratum by at- those of ampullate gland spigots. tachment discs, the dragline allows the spider to return safely to the starting point after a thrust at prey or following a free fall. Due to the impor- Discussion tance they have in the spiders’ lives, these fibers are also referred to as lifelines (Osaki 1996). Drag- In recent years, several traits of troglobiobiomor- lines are usually recycled by spiders (Vollrath phism have been described in arachnids. . They 1987, Hajer et al. 2011), because of their high nutri- include eye reduction or loss (Ćurčić et al. 2013), tional value (Miyashita et al. 2004). It has been appendage elongation, a reduction of cuticle pig- shown that in the troglobitic spider species Troglo- mentation (Arnedo et al. 2007), a reduction in neta granulum Simon, 1922 (Mysmenidae) drag- Spinning organs of Rhode aspinifera 137 lines help in navigation in an aphotic environment Systematics and evolution of troglobitic spiders of the genus Dysdera (Araneae, Dysderidae) in the Canary Islands. and allow females to maintain permanent contact Invertebrate Systematics 21: 623–660. with the cocoon containing eggs (Hajer & Řehák- Culver, D.C., Sket, B. (2000): Hotspots of Subterranean Biodiversity ová 2003). in Caves and Wells. Journal of Cave and Karst Studies 62(1): 11- 17. 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AES Bioflux 5(3): 306-315. Foelix, R.F. (2011): Biology of Spiders, 3rd ed. New York: Oxford silk threads inside the retreat. The newly hatched University Press. 419p. spiderlings stay with their mother and use the re- Glatz, L. (1972): Der Spinnapparat haplogyner Spinnen (Arachnida, treat for the first few weeks. The silk material used Araneae). Zeitschrift für Morphologie der Tiere 72: 1-50. Hadley, N.F., Ahearn, G.A., Howarth, F.G. (1981): Water and for the walls of the retreat is provided by the metabolic relations of cave-adapted and epigean lycosid spiders pseudaciniform glands, which spigots are located in Hawaii. Journal of Arachnology 9: 215–222. on the posterior median and posterior lateral Hajer, J., Řeháková, D. (2003): Spinning activity of the spider Trogloneta granulum (Araneae, Mysmenidae): web, cocoon, spinnerets (Glatz 1972, Hajer et al. 2013). 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