Table Of Content2001. The Journal of Arachnology 29:354-366
UNDER THE INELUENCE: WEBS AND BUILDING BEHAVIOR
OE PLESIOMETA ARGYRA (ARANEAE, TETRAGNATHIDAE)
WHEN PARASITIZED BY HYMENOEPIMECIS ARGYRAPHAGA
(HYMENOPTERA, ICHNEUMONIDAE)
William G. Eberhard: Smithsonian Tropical Research Institute, and Escuela de
Biologfa, Universidad de Costa Rica, Ciudad Universitaria, Costa Rica, email:
@
archisepsis biologia.ucr.ac.cr
ABSTRACT. On the evening that it will kill its host, the orb-weaving spider Plesiometa cirgyra, the
larva of the ichneumonid wasp Hymenoepimecis argyraphaga induces the spider to perform highly ste-
reotyped construction behavior and build an otherwise unique “cocoon web” that is particularly well-
designed to support the wasp larva’s cocoon. Cocoon web construction behavior is nearly identical with
the early steps in one subroutine of normal orb construction, and is repeated over and over. Usually all
other normal orb construction behavior patterns are completely or nearly completely repressed. Experi-
mental removal of the larva one or a few hours before cocoon construction would normally occur is
sometimes followed by nearly normal cocoon web construction, and sometimes by construction of other
highly altered web designs. The mechanism by which the larva induces these changes in the spider’s
behavior is thus apparently a fast-acting chemical, with effects that are manifested gradually. Partial
recovery of orb designs sometimes occurred several days later.
Keywords: Parasite, manipulation of host behavior, orb construction behavior, Plesiometa, Hymenoe-
pimecis
Manipulation of host behavior by parasites most finely directed alteration of host behav-
is a widespread phenomenon (Holmes & ior ever attributed to an insect parasitoid.
Bethel 1972; Moore 1984; Barnard & Behnke It has long been known that psychotropic
1990; Toft et al. 1991; Godfray 1994; Mc- substances can modify the forms of orb webs
Lachlin 1999; Poulin 2000), but most reports (Witt et al. 1968), but the details of how par-
of behavioral modifications, especially those ticular steps of the spider’s construction be-
caused by insect parasitoids in other insects, havior are affected have never been deter-
involve only simple behavior patterns such as mined. Elucidation of which aspects of
movement from one habitat to another, adop- behavior are changed can have important con-
tion of sleeping postures, or eating more or sequences for the common use of details of
less (Wickler 1976; Godfray 1994; McLachlan building behavior as taxonomic characters
1999). Spider behavior is also influenced by (Eberhard 1982; Hormiga et al. 1995; Gris-
insect parasitoids (Schlinger 1987). At least wold et al. 1998), as well as how evolutionary
some of these changes may be due to rela- transitions may have occurred. It has not al-
ways been clear whether or not some variant
tively simple mechanisms, such as modifica-
behaviorpatterns should be recognized as sep-
tion ofparticular receptors (Jenni et al. 1980).
arate traits (Eberhard 1990). If particular be-
This report concerns an unusually selective
havior patterns can be selectively induced,
behavioral modification by the larva of the then the case for their independence from oth-
parasitoid wasp Hymenoepimecis argyrapha- er traits, and thus their potential usefulness as
ga Gauld (Ichneumonidae), which apparently characters, is strengthened. Clarification ofthe
chemically induces expression of the early behavioral effects of this wasp parasite on
steps of one subroutine of orb web construc- web construction behavior thus promises to
tion in the spider Plesiometa argyra (Wal- improve understanding of the organization of
ckenaer 1841) (Tetragnathidae), while sup- behavior within the spider, and of the useful-
pressing all the rest of orb construction ness of different behavioral characters in spi-
behavior (Eberhard 2000a). It may be the der taxonomy.
354
EBERHARD—PARASITE MODIFICATION OF CONSTRUCTION BEHAVIOR 355
The life cycle ofH. argyraphaga is the foF
lowing (Eberhard 2000b). The female wasp
attacks P, argyra as the spider rests at the hub
of its orb, stings it into a temporary (10-15
min.) paralysis, and glues an egg to the spi-
der’s abdomen. Subsequently the spider resu-
mes normal activity, and builds apparently
normal orbs to capture prey during the next
approximately 7-14 days while the wasp’s egg
hatches and the larva grows. The larva re-
mains attached to the surface ofthe abdomen,
and feeds by sucking hemoiymph through
small holes it makes in the spider’s abdominal
cuticle. The second instar larva, on the night
that it will kill its host, induces the spider to
construct an otherwise unique “cocoon web”
of dragline silk, molts to the third instar, and
then kills and consumes the spider. The next
evening the larva spins a cocoon hanging by
a line from the cocoon web. The larva (which
is barely visible through the thin v/alls of the
cocoon) pupates about 4 days later, and then
emerges as an adult wasp after about 7 more
days. —
Figure 1. Web of an ueparasitized adult Pie-
METHODS siometa argyra. Scale bar = 3.0 cm.
Field observations were made near Parrita,
Puntarenas Province, Costa Rica (elev. 10 m) served after the spiders had been taken to San
in January and February of 1999 and 2000 in Antonio de Escazu (elev. 1300 m), where they
a mature plantation of African oil palm were kept indoors at room temperature for up
{Elaeis guineensis L.) where spider popula- to two weeks. On the evening the larva was
tions were dense. Web measurements were to be removed, the spider was kept in a small
performed in the morning, and thus did not container (6 cm dia.) in which it could not
include webs built later in the day (which may spin a web, and then placed on a wire frame
have different designs—Eberhard 1988). Con- as soon as the larva was removed between
struction ofcocoon webs made by spiders car- 2100 and 0200 h. Because the spiders seemed
rying wasp larvae was observed indoors near to need air movement to induce web construc-
Parrita the night after the spiders were col- tion, they were not kept in cages, but allowed
lected and transferred onto silk lines from P. to range freely in rooms.
argyra orbs that had been fastened to approx-
m RESULTS
imately horizontal 0.6 dia. circular wire
frames that were hung about 1 m above the FieM.^The orbs of spiders carrying wasp
floor. Larvae, which would kill their hosts that eggs and larvae were not distinguishable from
evening, could be reliably distinguished (15 of the more or less horizontal, moderately open-
15 cases) from others on the m.orning and af- meshed orbs of unparasitized spiders (Figs. 1,
ternoon of the same day, due to their larger 2) (ANCOVA analyses showed no significant
size. Voucher specimens ofwasps and spiders effects ofparasitism by larvae, or by eggs and
have been deposited in the U. S. National Mu- larvae {P = 0.91, 0.40). Even parasitized spi-
seum of Natural History, the Museum of ders found the morning of the day on which
Comparative Zoology at Harvard, and the they would be killed by the wasp larva were
Museo de Eetomologia of the Universidad de on freshly made, apparently normal orbs. Oth-
Costa Rica. er than orbs, the only other webs on which
The behavior of spiders from which the lar- unparasitized spiders occurred were small
va had been experimentally removed was ob- molting webs (Eberhard et al. 1993). These
356 THE JOURNAL OF ARACHNOLOGY
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20
20 30
Number
of radii
—
Figure 2. Numbers ofradii and sticky spiral loops (mean number ofloops directly above, below, and
to the sides ofhub) in webs of spiders in the field that were parasitized (filled symbols) and unparasitized
(open symbols). No differences between parasitized and unparasitized individuals were apparent.
webs were rare, and several newly molted in- More than 100 cocoon webs were observed
dividuals lacked such webs. Despite the dense in the field. They almost always consisted of
spider populations, no egg sacs or webs as- a few lines that radiated in a more or less hor-
sociated with egg sacs were seen; egg sacs izontal plane from a “hub” or central area,
may be hidden in leaf litter, as in the closely where the cocoon’s suspension line was at-
related Leucauge mariana (Keyserling) (Ibar- tached, and were each attached directly to a
ra et al. 1991; V. Mendez pers. comm.). support (Eberhard 2000a, Figs. 3-5). Most ra-
EBERHARD—PARASITE MODIFICATION OF CONSTRUCTION BEHAVIOR 357
—
Figures 3-5. Typical cocoon web. 3. Dorsal view. Scale bar = 3.0 cm; 4. Detail of attachments to a
leaf. Scale bar = 0.5 cm; 5. Lateral view. Scale bar = 3.0 cm.
358 THE JOURNAL OF ARACHNOLOGY
dial lines had many branches near their tips moved directly from one attachment to the
and were thus attached at many adjacent next as in normal frame and radius construc-
points to the substrate (Fig. 4). They were also tion.
sometimes attached at multiple points in the Radial lines were all in nearly the same
central area. There were several other indica- plane and were added to the web using two
tions, in addition to the planar arrangement of similar, simple behavior patterns (Fig. 8, A
radial lines, that the webs from which cocoons and B). The spider began by attaching its
were suspended represented modified orbs. dragline at the hub, then walked toward the
Some cocoon webs had circular lines similar substrate along a radial line, walked along the
to those at the hubs of normal orbs (17% of substrate a short distance and attached the line
41 webs checked for this detail) (Figs. 6, 7), it had laid from the hub (Aj, Bj). Then it re-
though in no case was the central portion of turned to the hub, laying a second dragline as
the hub empty, as in normal orbs. Some had it walked along this line or another radial line
one or more frame lines connecting the radial that it had laid previously and attached it at
lines (29% of42 webs checked for this detail) the hub (A2, B2). When the substrate was thin
(Fig. 6). These frames were typically much (a strand of wire, for instance) the spider usu-
shorter and nearerthe hub than were the frame ally moved to the opposite side to make the
lines of normal orbs (Fig. 1). The most elab- attachment before returning to the hub, as is
orate cocoon web had a distinct hub, frame typical of frame construction in orbs (Tilquin
lines, and a mesh above and below the hub. 1942; Eberhard 1990).
At the opposite extreme, the two simplest co- The two patterns differed in that either the
coon webs consisted of a single strong line lines were laid without attachments to previ-
with the larva or the cocoon hanging from the ously laid radial lines (A,, A2 in Fig. 8), or
central portion. (more often) the spider attached its dragline
Cocoon webs spanned smaller spaces than one or more times to radial lines both on the
normal orbs of mature females. The distance way out and on the way back to the hub (B,,
between the two most distant points ofattach- B2 in Fig. 8). Consecutive radial lines were
ment of anchor lines was smaller in cocoon always laid in different directions, as in orb
webs (mean 36.6 ± 17.2 cm in a sample of construction by other araneoid spiders (Ti-
38) than in orbs (99.6 ± 47.5 cm in a sample lquin 1942; Dugdale 1969; Le Guelte 1966;
of 31) {P < 0.001 with Mann Whitney U~ Witt et al. 1968; Eberhard 1982). Each radial
Test). These cocoon webs also had fewer an- line was reinforced repeatedly, and the total
chor lines (lines directed to the substrate) amount ofdragline silk in a cocoon web prob-
(mean 3.9 ±1.5 for cocoon webs, 5.3 ± 1.7 ably represented a major fraction ofthat in an
for the orbs; P < 0.001 with Mann-Whitney orb. The estimated total numbers of radial
U-Test). — lines in two finished cocoon webs were 36 and
Construction behavior. Cocoon web 30. Thus the number ofradial trips was on the
construction behavior, observed in five spiders same order as the typical number ofradii (20-
captured in the field the same day with larvae 35) in a normal orb (Fig. 1).
and a sixth three days after being collected, The behavior ofone further individual, col-
was very consistent. Early in the evening, the lected four days previously and observed in
spider built several lines, repeatedly removing San Antonio de Escazu, was very different.
and shifting the points of attachment as typi- The spider descended to the floor about 1.5
cally occurs during the preliminaries of orb below the wire hoop, formed a “hub” where
construction of many species of orb weavers several lines converged about 1 cm above the
(Tilquin 1942; Eberhard 1990). It then re- floor, and then made 5-10 very long radial
m
mained more or less immobile until between excursions (up to 1.3 each) walking on the
23:30 and 01:00, when construction activity surface of the floor. As it moved away from
occurred in bursts. Typically the spider added the hub it walked in a nearly straight line, at-
one to several radial lines in quick succession, taching its drag line periodically to the floor,
and then spent a minute or more (up to 30 but in some cases it gradually made an arc of
min) immobile at the hub before the nextburst up to more than 180° before it turned back
of activity. The spider's movements showed and slowly retraced its path back to the hub.
no signs of weakness or vacillation, and it On at least four occasions the spider encoun-
EBERHARD—PARASITE MODIFICATION OF CONSTRUCTION BEHAVIOR 359
—
Figures 6-7. Dorsal view of an unusually elaborate cocoon web with hub loops and a frame line.
Scale bars = 2.5 and 1,0 cm respectively.
360 THE JOURNAL OF ARACHNOLOGY
—
Figure 8. Diagrammatic representations ofthe sequences ofbehavior during construction ofa cocoon
web (A1-A2, and B1-B2) and a frame line in a typical orb (C1-C4). Stippling represents substrate, black
spots represent points where the dragline was attached, and dashed lines represent lines laid earlier in the
sequence (C,-C4 after Eberhard 1990). Cocoon web construction corresponds to the behavior in Cj and
the first part of C2.
EBERHARD—PARASITE MODIFICATION OF CONSTRUCTION BEHAVIOR 361
strate, and more or less converged at the hub
(Figs. 10, 11). A fourth spider, which had al-
ready begun cocoon web construction when I
removed the larva, resumed cocoon web con-
struction but did not return consistently to the
hub, and made two additional “hubs”. Sim-
plified, “vestigial” webs, that had only a few
more or less radial lines converging at the
point where the spiderrested and large masses
of silk lines loosely packed together near the
central area, were built by 13 spiders (Figs.
12, 13). These radial lines were attached to
the substrate at only one or at most a few
points. Vestigial webs never had hub loops,
temporary spirals or sticky lines, and only sel-
dom had recognizable frame lines. One further
web was a nearly normal orb, except that the
— center of the hub was not removed and some
Figure 9. Dorsal view ofa web made by a ma-
ture male on the night that it was killed by a wasp portions of the sticky spiral lacked sticky
larva. Note multiple attachments to substrate of balls.
some radial lines (as in Figs. 4 and 10). Scale bar The construction behavior of spiders from
= 3.0 cm. which larvae had been removed was observed
for two cocoon webs and three vestigial webs.
Cocoon web construction was very similar to
tered an object that it could have climbed and that described above for spiders carrying lar-
thus have raised its drag line offthe floor, but vae, including the frequent pauses between
instead it struggled on across the floor. When bursts ofconstruction behavior, except that on
I then removed the larva, and replaced the spi- some occasions the spider failed to attach its
der on the wire hoop after breaking the lines drag line at the hub when it returned after lay-
leading downward toward the floor, the spider ing a radial line. The drag line laid on the next
again descended to the floor where it made trip away from the hub was thus not attached
another hub. at the hub, but originated part way out the
Wasps generally avoided parasitizing ma- previous radial line (line 2~4 in B ofFig. 14).
2
ture males (Eberhard 2000), but two larvae on When this behavior was repeated over and
mature males matured and made cocoons in over, the hub gradually expanded and became
captivity. One male spider did not make a co- dispersed. The resulting web had large num-
coon v/eb (or indeed any supporting structure bers of more or less radial lines attached to
whatsoever); the wasp’s cocoon hung from a the substrate close to each other, but a diffuse
single short strand of spider silk. The second central area (Fig. 15).
parasitized mature ro.ale spider, however, built During vestigial web construction, the spi-
an extensive web that resembled a cocoon der also made radial lines attached to the sub-
web in being more or less planar, and having strate just as above. On some return trips to
many attachments to the substrate on the eight the hub area, however, it broke and removed
that it was killed and consumed by the larva these lines, reeling them up and leaving them
(Fig. 9). — packed loosely together attached to the web.
Experimental removal oflarvae. Larvae The final product ofthis process ofrepeatedly
were removed from 22 spiders in captivity on laying and then removing lines was a scanty
the evening when the spider was to be killed. array of more or less radial lines, and one or
Four spiders built no webs that night. The 18 more large masses of fluff (Fig. 13).
webs that were built were of three types. None of the 22 experimental spiders that
Three were more or less typical cocoon webs, built webs died on the evening the wasp larva
with a low number ofradial lines which were was removed. In nine cases the spider built a
composed of multiple strands that were at- second web on the following night, and the
tached at many adjacent points on the sub- second web was of the same type built on the
362 THE JOURNAL OF ARACHNOLOGY
—
Figures 10-13. Webs made by spiders from which the wasp larva was removed on the night when
the larva would have normally killed the spider. 10. Cocoon-web type, in which the few radial lines each
had multiple attachments to the substrate. Scale bar = 3.0 cm. 1 1. Close-up of hub of web in Fig. 10.
Scale bar = 1.0 cm. 12. “Vestigial” type web, in which a few radial lines were attached singly to the
substrate (heavy white lines are from previous web of another spider). Scale bar = 3.0 cm. 13. Close-up
of the hub of a vestigial web (different web from that in Fig. 12), showing several masses of fluff. Scale
bar = 1.0 cm; all wire hoops were horizontal.
first (two cocoon webs, seven vestigial webs). construction, however, which sometimes oc-
Five of the second vestigial webs had at least curs as part of frame construction, the early
one hub loop. Due to deaths and emigrations, stages do not involve removing or shifting
it was not possible to follow the spiders’ be- lines (Eig. 8 C,, C2). Premature termination of
havior systematically on subsequent nights. this type offrame construction behavior when
Two spiders survived for a week, and gradu- the spider returns to the hub after the first at-
ally built webs that were progressively more tachment to the substrate and followed by at-
orb-like though still substantially altered (Fig. tachment of the spider’s drag line at the cen-
16). tral area (x in Eig. 8 C2), would result in a
A
sequence ofoperations identical to type co-
DISCUSSION
coon web construction (Fig. 8 A). Adding at-
Comparison of cocoon web construction tachments to the line already in place on the
behavior with the early stages of normal orb way out would result in a sequence similar or
construction (Eberhard 1990) indicates that it identical to the second type of cocoon web
is probably homologous with the early steps construction behavior (Fig. 8 B). Similar at-
of type “D” frame construction (Fig. 8 Cj- tachments sometimes occur in the closely re-
C4). Most anchor line construction in an orb lated L. mariana during frame construction of
involves removal of lines already in place, or types “A” and “C” of Eberhard (1990) but
shifting their attachments to each other (Ti- were not seen in conjunction with type D of
Iquin 1942; Eberhard 1990), but neither of Eberhard (1990) (the same individual often
these behavior patterns was ever seen during performed more than one type while building
cocoon web construction. In type D anchor a given orb). A further resemblance to attach-
EBERHARD—PARASITE MODIFICATION OF CONSTRUCTION BEHAVIOR 363
—
Figure 15. Cocoon-type web with dispersed
hub built by a spider from which the larva was
removed on the evening on which it would have
Figure 14.—Diagrammatic representations ofco- normally killed its host. Scale bar = 3.0 cm; wire
coon web construction behavior of a spider with a hoop was horizontal.
wasp larva (Aj, A2) and a spider from which the Figure 16.—Orb-like web built by a partially re-
wasp larva had been experimentally removed (Bi, covered spider. The wasp larva had been removed
B2). The experimental spidersometimes omittedthe five days earlier, on the eveningwhenitwouldhave
cFfiiongna.slt8rautcAtta2icoahnmned(natBtt2aa)t;chtwmhheenethnu3bititmnyopAiviceadlanoadfwaAcyo2c;fosroeonemwatlehsbeo kvielsltiegdiatlhewsepbideorn, tahnadt ntihgehts.piSdcearlehabdarsp=un2.a0tcympi.cal
hub to make the next radial line, the dragline was
thus displaced away from the hub (line 2-4 in Bj). ther evidence that cocoon webs were homol-
Rdiefpfeuasteecdenotmriaslsairoenasoofftthheiswaetbta(cFhimge.nt15r)e.sulted in a ogous with orbs is the fact that when these
webs had more than three radial lines, these
were nearly always in approximately the same
ments of anchor lines built during orb web- plane. In addition, some cocoon webs had
construction by other orb weavers (Tilquin frame lines, and a few had hub loops (Figs. 6,
1942: Eberhard 1990) was the attachmeet of 7).
radial lines to thin objects by moving to the The homology ofcocoon and orb webs em-
opposite side of the object just before attach- phasizes that perhaps the most extraordinary
ing. Thus, the spider built the cocoon web by aspect of the wasp larva’s effect on the spider
apparently repeating the first portions of one was not so much what the spider did, but what
type offrame construction over and over. Fur- it did not do. Many aspects ofnormal orb con-
