EXTERNAL MORPHOLOGY AND ULTRASTRUCTURE OF THE PREHENSILE REGION OF THE LEGS OF LEIOBUNUM NIGRIPES (ARACHNIDA, OPILIONES)

6 Pages·2000·5.7 MB·English

by  Cary Guffey

2000. The Journal of Arachnology 28:231-236
RESEARCH NOTE
EXTERNAL MORPHOLOGY AND ULTRASTRUCTURE OF
THE PREHENSILE REGION OF THE LEGS OF
LEIOBUNUM NIGRIPES (ARACHNIDA, OPILIONES)
Keywords! Chemoreception, harvestmen, locomotion, setae
Species of harvestmen (Arachnida, Opili- leg are traversed by two tendons arising from
ones, Palpatores) in the family Sclerosoma- muscles that are used to move the tarsal claw.
tidae frequently employ prehensile flexion of The telotarsus is subdivided by numerous
the telotarsus during locomotion. Kaestner adesmatic joints (>50: Kaestner 1968) that
(1968) described the ability of these arach- impart a prehensile character to the tarsus
nids to anchor themselves to objects such as when flexed (Figs. 5-7). Flexion at the ades-
blades ofgrass by wrapping their legs around matic joints can occur only ventrally in L. ro-
these objects. We have observed both Leiob- tundum (Latreille 1795) because the ventral
unum nigripes (Weed 1892) and L. vittatum joint membranes are shorter than the dorsal
(Say 1821) moving across surfaces by form- joint membranes (Kaestner 1968). In this pa-
ing coils at the end of their legs, especially per we describe the external morphology and
the second pair (Figs. 1-4). While moving ultrastructure of the prehensile region of the
across a smooth substrate, these harvestmen legs ofjuveniles ofLeiobunum nigripes (Scle-
cast the coiled regions oftheir legs about un- rosomatidae).
til they catch on a structure. Similar strate- We collected juvenile Leiobunum nigripes
gies are also employed by harvestmen during from Chicot State Park, Evangeline Parish,
climbing, with the exception being that once Louisiana on 8 March 1997 and housed them
a purchase is obtained with a coil, the free in screened aquaria for approximately one
legs often wrap around and climb up the an- week prior to preservation. Within 48 h after
chored leg. In addition, we have also ob- molting, specimens were fixed in cold (4 °C)
served harvestmen in aggregations wrapping
Trump’s fixative (a mixture of sodium caco-
their legs around the legs of adjacent indi-
dylate buffer, formalin, and glutaraldehyde)
viduals (Fig. 2). overnight, rinsed in 0.2 M sodium cacodylate
Movement of the legs in harvestmen has buffer (pH 7.4) and postfixed in 2% OSO4
been hypothesized to occur through a combi-
nation of muscle action and a hydraulic pump for 90 min at room temperature. Specimens
were then dehydrated in a graded ethanol se-
mechanism (Shultz 1989; Foelix 1996). Ac-
cording to this hypothesis, hemolymph is ries and chemically dried with hexamethyldi-
pumped into the legs by contraction of either silazane (Nation 1983), mountedon aluminum
the musculi laterales or the endostemal mus- stubs, and sputter-coated for 2 min with —20
nm of gold. We examined and photographed
cles (the primitive condition: Shultz 1991) of
the prosoma (Parry 1960), resulting in leg ex- these specimens with a JEOL 6300-F field
tension. For harvestmen, Shultz (1989) re- emission scanning electron microscope at ac-
ported that the basitarsus and telotarsus ofthe celerating voltages of 15-20 kV.
Specimens examined with transmission
^Current address: Department of Biology, 411 electron microscopy (TEM) were fixed and
SW 24th Street, Our Lady of the Lake University, dehydrated using the same protocol described
San Antonio, Texas 78207-4689, USA. above for scanning electron microscopy
231
232 THE JOURNAL OF ARACHNOLOGY
iungB!>S
»8S^
Figures 1-4.—Adults of the harvestman Leiobunum nigripes on hardware cloth (mesh size 6 mm X 6
mm) showing the prehensile ability of the tarsi. 1. An individual anchored to the substrate; 2. A small
aggregation ofharvestmen in which one individual has wrapped one of its leg around the leg ofanother;
3, 4. Dorsal views ofthe prehensile region ofthe tarsi, showing the wrapping ofthe legs aroundindividual
metal wires. Arrows in each figure indicate regions of flexion in the distal tips of the telotarsus.
(SEM). Following dehydration, specimens basal articulating membrane (Figs. 6, 7). The
were slowly infiltrated in Spurr’s low viscosity sensilla chaetica are nearly perpendicular to
standardresin (Spurr 1969) overfourdays and the leg surface and have a specialized basal
sectioned with a diamond knife. Thin sections articulating membrane (Figs. 11, 12), with
were collected on carbon-stabilized 200 iJim blunt tips and whorled striae (Fig. 14), unlike
thin bar grids, stained sequentially with meth- those of sensilla trichodea (Figs. 6, 7). There
anolic uranyl acetate and aqueous lead citrate, is no evidence of trichobothria, mechanore-
and observed with a Hitachi H-7000 trans- ceptors that are common to most arachnids
mission electron microscope at 75 kV. (Reissland & Corner 1986; Foelix 1996). The
On each leg, L. nigripes has a single, adesmatic joints are easily distinguished from
smooth tarsal claw that is not toothed (Fig. 5). true joints (Fig. 8) on the basis of their small
Smaller setae, or sensilla trichodea (Schneider size.
TEM
1964; Spicer 1987), and largerprimary spines, Cross sections examined with con-
or sensilla chaetica (Schneider 1964; Spicer firmed the earlier anatomical observations of
1987), are denser on the ventral surface ofthe Kaestner (1968); i.e., no muscles were found
telotarsus than on the dorsal surface (Fig. 6). between the segments of the telotarsus (Fig.
The sensilla trichodea lie nearly parallel with 9). We observed only a single tendon (Fig. 9)
the surface of the leg and have no specialized connecting the tarsal claw to the claw-flexing
GUFFEY ET AL.—PREHENSILE REGION OF HARVESTMEN LEGS 233
—
Figures 5-8. Externalmorphologyoftarsus IVofLeiobunumnigripes. 5. Lateralviewofthetelotarsus
and tarsal claw. Scale bar = 127 mm; 6. The adesmatic joints on the ventral surface of the telotarsus.
Scale bar = 64 pm; 7. The sensilla trichodea (st) and sensilla chaetica (sc) on the ventral surface of the
telotarsus near an adesmatic membrane (am) ofan adesmaticjoint. Scale bar = 23 pm; 8. A lateral view
of a truejoint between the two most distal segments of a leg, the basitarsus and the telotarsus. Scale bar
= 73 pm.
musculature located in the tibia. In the telo- do not attach to the cuticular wall ofthe bas-
tarsus, we also observed epidermal cells lining al articulating membrane. Instead, the sheath
the innermost portions of the cuticle (hypo- containing the dendrites passes directly
dermis) and occurring in clusters within the through the center ofthe setal shaft (Fig. 12,
leg hemocoel (Fig. 10). 13), a common feature of arthropod che-
During the course of our TEM studies of moreceptors (Altner & Prillinger 1980; Za-
the internal features of the leg, several sec- charuk 1980).
tions provided information concerning the The external morphology of the prehensile
innervation of the sensilla chaetica (Figs. 6, region of the legs of Leiobunum nigripes is
7, 11). Apical pores, a common feature of similar to that reported by Kaestner (1968) for
sensilla chaetica among arthropod chemo- L. rotundum and by Holmberg & Cokendol-
receptors (reviewed in Zacharuk 1980), pher (1997) for Togwoteeus biceps (Thorell
were not observed in our specimens. This 1877). Our observations ofthe sensilla on the
sensillum is innervated by many presumably tarsi of L. nigripes are also similar to those
chemoreceptive dendrites (Figs. 12, 13). The reported by Spicer (1987) for the palps of L.
dendrites originate from enveloping cells townsendi. The most numerous sensory or-
within the hypodermis (Fig. 13; inset) which gans on the legs of L. nigripes appear to be
234 THE JOURNAL OF ARACHNOLOGY
—
Figures 9-14. Ultrastmcture of the telotarsus of leg IV of Leiobunum nigripes. 9. TEM micrograph
ofacross sectionofthetelotarsus revealing asingletendon (t)within ahemocoelic space (hs) andshowing
no muscle or tendon attachments with the inner surface of the cuticle (c). Scale bar = 6 pm; 10. TEM
micrograph ofthe epidermal cells lining the innermost portion ofthe cuticle. Scale bar = 3 pm; 11. SEM
micrograph ofthe specialized basal articulating membrane (bm) ofa sensilla chaetica (s) from the ventral
surface of the telotarsus. Scale bar = 3 pm; 12, TEM micrograph of a basal articulating membrane and
shaft of a sensilla chaetica revealing the dendrites (d) and dendritic sheath (ds) within the shaft of the
GUFFEY ET AL.—PREHENSILE REGION OF HARVESTMEN LEGS 235
sensilla chaetica (primary spines) and sensilla LITERATURE CITED
trichodea (setae). Unlike the palps ofL. town- Altner, H. & L. Prillinger. 1980. Ultrastmcture of
sendi, however, these sensilla appear to be invertebrate chemo-, thermo-, and hygrorecep-
more numerous on the ventral surface of the tors and its functional significance. Int. Rev.
telotarsus than the dorsal surface. Spicer CytoL, 67:69-139.
(1987) also reported two types of sensilla Foelix, R.F 1985. Mechano- and chemoreceptive
chaetica (types I and II) based on the differing sensilla. Pp. 118-137, In Neurobiology of
lengths of the sensilla. We observed only one Arachnids. (EG. Barth, ed,). Springer-Verlag,
type of sensilla chaetica in L. nigripes. We Berlin.
also did not observe any pores that are char- Foelix, R.F. 1996. Biology ofSpiders, 2nd ed. Ox-
ford Univ. Press, New York.
acteristic of chemoreceptors on the sensilla Holmberg, R.G. & J.C. Cokendolpher. 1997. Re-
chaetica (Slifer 1970), but the structure ofthe
description of Togwoteeus biceps (Arachnida,
dendrites innervating them (e.g., many den- Opiliones, Sclerosomatidae) with notes on its
drites and lack of attachment to the basal ar- morphology, karyology andphenology. J. Arach-
ticulating membrane) indicates that they may nol., 25:229-244.
function in chemoreception. Spicer (1987) in- Kaestner, A. 1968. Invertebrate Zoology, Vol. II:
ferred that the row ofspines found on the ven- Arthropod Relatives, Chelicerata, Myriapoda.
tral surface of the palps ofL. townsendi were (Translated by H.W. Levi & L.R. Levi.) Intersci-
chemoreceptors and such receptors have been ence Publishers, New York.
reported for other species ofharvestmen (e.g., Nation, J.L. 1983. A new method for using hexa-
methyldisilazane for preparation of soft insect
Foelix 1985).
tissue for scanning electron microscopy. Stain
ACKNOWLEDGMENTS TechnoL, 58:347-351.
Parry, D.A. 1960. Spiderhydraulics. Endeavor, 19:
Funding for this study was provided by a 156-162.
grant to C. Guffey from the American Arach- Reissland, A. & P. Gomer. 1986. Trichobothria. Pp.
nological Society Fund for Graduate Student 138-160, In Ecophysiology ofSpiders. (W. Nen-
Research, Louisiana Board of Regents Doc- twig, ed.). Springer-Verlag, New York.
Schneider, D. 1964. Insectantennae. Ann. Rev. En-
toral Fellowship grant LEQSF[1994-99]-GF-
tomoL, 9:103-122.
29 to C. Guffey through R.G. Jaeger, United Shultz, J.W. 1989. Morphology of locomotor ap-
States Department of Agriculture grant pendages in Arachnida: Evolutionary trends and
USDA-CREEF 9501834 to B.E. Felgenhauer, phylogenetic implications. Zool. J. Linn. Soc.,
and research grants from The University of 97:1-56.
Southwestern Louisiana Graduate Student Or- Shultz, J.W. 1991. Evolution of locomotion in
ganization to C. Guffey and V.R. Townsend. Arachnida: The hydraulic pressure pump of the
Assistance with the identification of species giant whipscorpion, Mastigoproctus giganteus
was provided by J. Cokendolpher. We thank (Uropygi). J. Morph., 210:13-31.
J. Marshall and two anonymous reviewers for Slifer, E.H. 1970. The structure of arthropod
chemoreceptors. Ann. Rev. Entomol., 15:121-
critically reviewing an earlier draft of this
142.
manuscript and T. Pesacreta for assistance Spicer, G.S. 1987. Scanning electron microscopy
with the transmission electron microscope and of the palp sense organs of the harvestman
the scanning electron microscope at the Elec- Leiobunum townsendi (Arachnida: Opiliones).
tron Microscopy Center at The University of Trans. American Microsc. Soc., 106:232-239.
Southwestern Louisiana. Spurr, A.R. 1969. A low-viscosity epoxyresinem-
<-
seta. Scalebar = 2 [xm; 13. TEMmicrographofasensillachaetica, thecuticle andtheunderlying structure
within the telotarsus. The inset is of a nerve from a chemoreceptive setae, revealing multiple dendrites
within a single dendritic sheath. Scale bar = 5 ixm; 14. SEM micrograph of the distal tip of a sensilla
chaetica revealing the whorled striae on the external surface and the lack ofa discemable pore at the tip.
Scale bar = 3 fxm.
236 THE JOURNAL OF ARACHNOLOGY
bedding medium for electron microscopy. J. Ul- Bruce E. Felgenhauer: Department of
trastruc. Res., 26:31-43. Biology, P.O. Box 42451, University of
Zacharuk, R.Y. 1980. Ultrastructure and function Southwestern Louisiana, Lafayette, Louisi-
ofinsectchemosensilla. Ann. Rev. EntomoL, 25: ana, 70504^2451 USA
27-47.
Manuscript received 18 December 1998, revised 5
Cary Guffey^ Victor R. Townsend, Jr., and January 2000.