BiologicalJournal
if the
Linnean So&@ ( 1998), 63: 205-2 19. With 6 figures
Factors influencing the evolution of social
behaviour in Australian crab spiders
(Araneae: Thomisidae)
THEODORE A. EVANS’
Department of <oologv, Uniuersip of Melbourne, Parkville, fictoria, 3052, Australia
Received 27 March 1997; acceptedfor Publication 28 August 1997
The social Diaea are non-territorial, periodically-social spiders that do not weave a snare
web, a factor considered to be important in spider sociality. Maternal care and heritable
retreats are factors common to most group living animals, including social h a ; suggesting
that they are important factors in the evolution of spider sociality. A 4 year survey, along
with field and laboratory experiments revealed that mother spiders provided crucial care in
the form of a protective Eucabptus leaf nest and large prey for their offspring. After the
mother’s death, the nest was inherited and expanded by the offspring. Larger groups built
larger, more protective nests, but expended less individual effort doing so, and so survived
better than smaller groups.
0 1998 The Linnean Society of London
ADDITIONAL KEY WORDS:*ommunal
behaviour - maternal care - protective retreat.
CONTENTS
Introduction . . . .
Material and methods
Survey data . .
Experimental data
Results . . . . .
Survey data . .
Discussion . . . .
Acknowledgements
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References . . . .
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205
207
207
207
209
209
215
217
217
INTRODUCTION
The discovery of South American spiders with ‘gregarious habits’ amazed Darwin
(1845: 37); since then some form of ‘gregarious habit’ has been found in over 100
spider species in 26 families (see Buskirk, 1981; D’Andrea, 1987; AvilCs, 1997 for
reviews). These social behaviours have been categorized using territorial aggression
’
Present address: CSIRO Division of Entomology, Canberra, ACT, 2601, Australia. Email: theo.
[email protected]
0024-4066/98/020205 t 15 825.00/0/bj970179
205
0 1998 The Linnean Society of London
206
T. A. EVANS
and the duration of the group; those considered to have the most derived social
state are non-territorial and permanently-social. Spiders that fall into this category
typically display social behaviours such as cooperative prey capture, communal
feeding and communal nest construction, and have some form of irregular snare
web (Shear, 1970; Burgess, 1976; Buskirk, 1981; D’Andrea, 1987; AvilCs, 1997).
Unlike social spiders from other families, Diaea socialis Main (Main, 1988), D.
qandms Evans and D. mgagyna Evans (Thomisidae)(Evans, 1995)and Delenu cancerides
Walckenaer (Sparassidae) (Rowell & AvilCs, 1995) are from families that do not
weave any form of snare web, a behaviour considered to be important in the
evolution of sociality in spiders (see above reviews). The absence of snare web
weaving in Diaea and Delaa suggests that the adaptive significance of their social
behaviour cannot be explained easily in the existing classifications of social spider
behaviour. This study deals with Diaeu egundms, an annual species that inhabits
Eucubptus forests in south-eastern Australia (Evans, 1997). In early summer, gravid
females migrate alone from their home nest to built a brood chamber from several
Eucabptus leaves, in which they lay a single eggsac of c. 45 (range 15-80) eggs. The
female continues to attach leaves to this brood chamber after her eggs hatch, and,
in autumn, is eaten by her offspring who then inherit her nest (Evans, 1995; Evans,
Wallis & Elgar 1995). The offspring remain together in the nest, continuing to add
leaves onto the nest, and foraging cooperatively from entrances on its surface. The
following spring, the offspring mature, and after mating, migrate to reproduce.
AvilCs ( 1997)classified Diaea as ‘technically’‘non-territorialperiodical-social’ because
the groups eventually disintegrate after mating as female spiders migrate alone to
found new nests. However, she noted that because Diwu groups persist after the
spiders mature that these species “appear to be at the transition point between
periodic- and permanent-sociality”.
Therefore, the social Diaea are well placed for investigation into factors that
promote extended group living in a typically solitary family. Work in other diverse
taxa has produced three factors suggested to favour the evolution of sociality: gradual
development, parental care and inhabiting a permanent, expandable and protective
retreat (Anderson, 1984; Alexander, Noonan & Crespi, 1991; Seger, 1991 ; Crespi,
1992; D u Q 1996; see also Seger & Moran, 1996). The maternal care exhibited by
thomisids may preadapt them to sociality. Female crab spiders often enclose their
eggsacs with vegetation and remain with them until they hatch (Bristowe, 1958).
This behaviour is exhibited by solitary a u e u and their close relatives Xysticus and
Cyrnbucha L. Koch that curl a single eucalypt leaf as a brood chamber (Main, 1988).
However, the social Diaea invest more energy in pre-oviposition preparation by
using four or more leaves, creating an incipient nest, before laying their single
eggsac, and post-oviposition care, behaviour not seen in solitary crab spiders.
The delayed (adult) dispersal seen in the social Diaea offspring, well past the
lifespan of the mother, suggests that other benefits must accrue to group living in
addition to those provided by the mother. One benefit might be the nest itself, as
a protective structure or foraging area. The nest attracts attention from potential
predators, including vertebrates such as birds and possums, and may be invaded by
commensals and other spiders such as Clubionia mbusta L. Koch, a common, barkdwelling spider. The constituent leaves are held together tightly, and their haphazard
arrangement is labyrinthine inside, features that may guard against such predators.
Here, I report on a long-term survey, two field and two laboratory experiments
that describe and investigate aspects of the life history of D . qandms. In particular,
SOCIAL CRAB SPIDERS
207
I investigated the influences of the mother on the survival and growth of her offspring
early in the life cycle, and also investigated the influence of group size on survival
and growth of ,group members, and on nest construction later in the life cycle (after
the mother’s death), so as to better understand the adaptive value of their social
behaviour.
MATEEUAL AND METHODS
Suwq data
I surveyed the demography of D. ergandms from nests collected from five sites in
Victoria, Australia, from March 1991 to August 1994. I chose the sites at Mt
Disappointment State Forest, Kinglake National Park, Yan Yean Water Catchment,
Brisbane Ranges State Park and Otways Ranges State Forest, due to their similarity
in floristic diversity, proximity, ease of access, low canopy (10-20 m) and low human
activity. I surveyed the field sites each month during this time, except for March-June
1993. I collected a total of 505 nests by either climbing the tree, or using secateurs
on an extending pole. These were bagged individually and transported to the
laboratory for dissection.
Animals found in the nest were separated into three categories: D. ergandms,
commensals and predators. The 1 1 52 1 (including 267 mothers) D. ergandros collected
were weighed and categorized by sex and developmental stage (adult, subadult and
juvenile). Adults were distinguished by their colour and developed genitalia (sixth
instar females and fifth instar males). Subadults could be determined from partially
formed genitalia (fourth and fifth instar females, and fourth instar males).Juveniles
were third and earlier instars, and it was not possible to determine their sex. I
defined commensals as those animals that D. ergandms neither attacked nor avoided
for 48 hours when contained together in jars in the laboratory. I identified animals
as predators when they were seen to eat D. ergandms, either in the field, or in the
laboratory. I found oophagous larvae or pupae in some eggsacs, and identified them
after the adults eclosed. I measured dry leaf weight (one week at RT, then 6 h at
150°C) of 374 nests.
I compared group size (excluding the mother if present), mean spider weight
(mean weight of spiders found in the nest, excluding the mother if present), adult
and subadult sex ratio (number of males divided by the total number of spiders),
nest size (dry weight of leaves), and construction activity broportion of green leaves
in the nest) with time of year and each other using Spearman’s correlation and
multiple regression analyses, the residual values (i.e. the deviation from the predicted
value) from the regressions were compared with t-tests to consider maternal or
predator effects. I performed the analyses on Systat for windows (Systat Inc.,
Evanston IL, USA). Variables were transformed logarithmically where necessary,
to achieve normal distribution and increase homogeneity of variances in order to
meet parametric analysis assumptions (Sokal & Rohlf, 1981).
Experimatal data
Efects of maternal care
I examined the influence of the mother and spiderling group size on the survival
and growth of spiderlings in a field experiment. I collected 35 nests from Yan Yean
208
T. A. EVANS
Water Catchment in November 1991, dissected them and counted and weighed the
spiders. The mother was present in 25 of the groups, and absent in 10. Group size
ranged from 12 to 64 spiderlings (mean+_ SE, 28.8 k2.7). I placed the groups (group
size not manipulated) into individual plastic vials (6.5 x 4.5 cm diameter) with an
artificial nest (four pieces of paper shaped like Eucahptus leaves enclosed within green
plastic shade-cloth ). The spiders were left in the plastic vials with the artificial nest
for one week to encourage weaving (after Evans & Main, 1993). I returned the
plastic vials to the collection site, removed the artificial nest without dislodging the
spiders, and attached it to a branchlet with several leaves using a twist tie. I
monitored the artificial nests during the day and night for activity, especially weaving,
foraging or dispersal, for 2 weeks. The experiment ran for 2 months, after which I
collected the nests, counted and weighed the surviving animals, and recorded data
on nest construction. Survival, growth and nest construction were compared using
Spearman’s correlation and multiple regression.
I examined the influence of the mother and of prey size on the survival and
growth of spiderlings in a laboratory experiment. I collected nests from Yan Yean
in March 1992, from which I assembled 48 replicate groups of 20 sibling spiderlings.
These were housed in plastic containers (20 x 10 cm diameter) with two pieces of
paper shaped like Eucalrptus leaves. Mothers, which were removed during nest
dissection, were returned to their offspring in 24 groups; the remainder did not have
a mother spider. Half the groups were fed small flies, Drosophila melanogaster, which
are smaller than spiderlings, the other 24 groups were fed large flies, Luciliu cuprinu,
which are larger than spiderlings. Spiders were fed twice a week with 52 D.
mehogaster or two L. m . m . This was considered to be equivalent available biomass
as 26 D.melunoguster (0.86 kO.01 mg, n=411) were not simcantly heavier from
one L. cuprinu (20.1 kO.18 mg, n=263) (461 = 1.95, P>0.05), but 27 D.melanogaster
were significantly heavier (461=2.15, R0.05). The upper limit was used in an
attempt to reduce any effects of a larger amount of inedible exoskeleton in D.
melunoguster (after Rypstra, 1993). I recorded prey capture, and removed all dead
and live flies before new flies were added. The experiment ended after 2 months
when I counted and weighed surviving animals, and calculated the volume of the
retreat constructed. I compared survival, growth and retreat size using two factor
ANCOVA, with mother presence and prey type as the two factors, and with initial
mean spiderling weight as the co-variate.
Efects o f p u p size
I examined the influence of group size on survival, growth and nest construction
behaviour of D. qundms in a field experiment. I collected nests from Healesville
Corrandirk Reserve in May 1991, dissected them, and counted and weighed the
spiders. The size of these natural groups (comprised mostly of third instar juveniles
and subadults) was not manipulated. Group size ranged from 6 to 70 spiders
(24.9 k 1.9, n=52). I followed the same experimental procedure as for the field
experiment above. I returned the artificial nests to the collection site, and monitored
them during the day and night for activity for 2 weeks. A severe storm occurred
during this time, so I noted damage to the nests, and re-checked them for signs of
activity. The experiment ran for 3 months, after which I collected the nests, counted
and weighed the surviving animals, and recorded the data on nest construction.
Survival, growth and nest construction were compared using multiple regression
against initial group size and initial mean spider weight.
SOCIAL CRAB SPIDERS
209
Nests as protective retreats
I examined the influence of predators on subadult spiders in a small laboratory
experiment. I collected 10 large nests from Yan Yean in October, 1992, and removed
30 spiders from each. I placed three ofthese groups into plastic containers (30 x 15 cm
diameter), with eight pieces of malleable, transparent, plastic shaped like Euca&~tus
leaves attached on the inside top surface. The other seven groups were held in
containers without nest-building material. After 1 week, spiders had constructed
nests using all plastic ‘leaves’.The spiders were clearly visible, often grouped together,
inside the nest. I fed all groups D. melanogasto and L. cuprina, and observed prey
capture similar to that seen in the fieM. I placed one Clubiona robusta (ca. 40g) into
each container after 3 weeks. The cohtainers were watched intensively for 48 hours
(including time-lapse video), then pe&odic observations followed. The experiment
ended after 4 weeks when I counted surviving animals.
RESULTS
Survey data
Solitary gravid females dispersed from their natal nests in late spring-summer
and began new nests. Mothers became lighter as autumn proceeded (Fig. lA), and
they were rarely found in nests collected in winter. The mean spider weight increased
with time of year peaking in spring, coinciding with maturation (Fig. 1A). Weight
differed between sex-classes; adult females (1 8.8 f 1.O 1 mg) were heavier than subadult females (1 1.9f0.44 mg) (ti43 = 5.98, PcO.00 l), similarly, adult males
(12.0 f0.66 mg) were heavier than subadult males (1 0.1 f0.29 mg) (ti38 = 2.55,
P C0.02).Females were heavier than males (ha3= 4.8, RO.001). The adult sex ratio
was extremely variable (range= 0.0-1 .O), especially in nests containing small adult
groups. However, the sex ratio in the younger and larger nests, containing mostly
subadult spiders, was close to parity (mean = 0.45 f0.015, n = 132). Group size was
highest in the summer after eggs hatched, and was smaller in the later months of
the year (Fig. 1B). There was a small, but significant trend for group size to decrease
as spider weight increased (Spearman’s correlation 12 = 0.10, PCO.001) (Fig. 1B).
Although nests began as a single leaf (c. 0.12 g), they could eventually contain as
many as 62 leaves (9.6g). Nest size varied over the time of year, the larger nests
were found in spring and summer (Fig. 1C). The proportion of green leaves in the
nest, a measure of construction activity, varied with time of year; the highest levels
were found associated with incipient nests in summer, and with older nests in spring
(Fig. 1D). A multiple regression shows that nest size increased with group size (Fig.
372 = 23 1.2, RO.001). The nests
2A) and mean spider weight (Fig. 2B) (r= 0.75, F2,
with mothers had a significantly lower residual (&=5.19, RO.001) (Fig. 2C)
suggesting that groups with mothers (of equal group size and mean spider weight)
contributed significantly less to nest construction, implicating mothers’ continued
contribution to nest building. Nests with predators had a significantly higher residual
(447= 2.25, PC0.05) (Fig. 2D), suggesting that spiders were contributing more to nest
construction when predators were present.
The mean contribution to nest construction per spider (nest weight/group size)
decreased with increased group size (r= 0.7 1, Fl, = 370.9, RO.001) (Fig. 3A),
T. A. EVANS
210
A
4Qr
B
C
1
D
p
6
(II
20
0
0.8
I-n - - -
E
I
1. 1
S O N D J F M A M J J A
Spring
Summer Autumn
Winter
Figure 1. The annual variation in natural Dim qundtus colonies. A, individual spider mass (mothers=
lilled columns, spiderlings and subadults=open columns).B, number of spiders in the group. C, weight
. of leaves comprising nest. D, Proportion of green leaves in the nest. E, number of predators found in nest.
SOCIAL CRAB SPIDERS
A
3r
21 1
B
r
-
tu
.
-7
-3
- 2 - 1 0 1 2 3 4
- 1 0 1 2 3 4 5
Ln group size
Ln mean spider mass (mg)
Absent Present
Mother
Absent Present
Predator
Figure 2. Natural nest size as a function of A, spider size and B, number of spiders in the group
(multiple regression: r = 0.74, y = 0.53 weight 0.30 group size - 1.04). The residuals of the multiple
regression compared between C, mother presence, and D, predator presence (see text).
+
0.8
A
3r
67
b
rn
8
3
3
8
21-
0-1-
-2
B
1
212
T. A. EVANS
suggesting that spiders in larger groups expended less effort in nest building. The
nests with mothers had a significantly lower residual (t373= 3.69, P<O.OOl) (Fig. 3B)
suggesting that mothers lowered significantlythe individual effort in nest construction.
Most Diaea qandms nests contained skeletal remains of prey, which could be
identified to order as thomisids do not masticate their prey. The most common prey
were beetles (Coeloptera),wasps and ants (Hymenoptera),but flies (Diptera), moths
(Lepidoptera) and damselflies (Odonata) were also found. Prey were often larger
than the spiders; some wasps had a body length five times longer than their captors.
Commensals included cockroaches (Blattoidea), psyllids (Hemiptera; Psyloidea),
woolly scale insects (Hemiptera; Coccoidea), and the adults and larvae of leaf-eating
beetles (Coeloptera; Chrysomelinae). Cockroakbes were more common in older,
larger nests with mostly dead leaves, whereas the psyllids, scale insects and beetle
larvae were common in younger, smaller nests on green leaves. No analyses were
performed on these data.
I observed three vertebrate predators investigating D. qandms nests in the
field two birds (Bell Miner, Manorina mlanophtys and Yellow-faced Honey-eater,
Lichenostomus chtysops), and one mammal (Feather-tailed glider, Acmbutes pygmaeus).
These species are small enough to reach the spider nest located on the distal end
of the branch. They were successful at infiltrating small, incipient nests (1-5 leaves),
but not older, larger nests. Laboratory trials I performed with A. pypueus were
consistent with these field observations. The gliders investigated five large nests
(210 leaves), but did not dislodge any leaves, whereas they successfully tore open
five small nests ( S5 leaves), and ate the spiders therein.
I found three species of oophagous larvae from 34 eggsacs in summer: Acanthostethus
sp. (Nyssoninae, Sphecoidea) was predominant, but a pompilid wasp and a fly
(species unknown) were found also. I found four species of vagrant spiders in 19%
of nests. Over 75% of these were Clubiona mbusta (Clubionidae); the remainder were
Lampona cylindrata (L. Koch) (Gnaphosidae) or two unidentified salticid species.
Predators were most abundant in the warmer months, particularly in older, larger
nests with maturing D. qandms (Fig. 1E). I observed C.mbustu eating D. qandms on
the surface of the nest several times in the field.
Efects of m a h a l care
In the field experiment, groups with mothers had a lower failure rate: 23 of the
25 groups with mothers persisted whereas only two of the 10 groups (total of four
spiders)without mothers persisted (Fisher’s exact <O.OOOO 1). Spiderlingsin motherless
artificial nests were observed abandoning the artificial nests during the first few days
after replacement in the field. Consequently, spiderling survival was higher in nests
with mothers (mean= 56.2 & 24.9?40) than without (mean= 1.O f2.1 %) (t33=6.94,
P <0.001). The proportion surviving was not affected by the initial group size (Fl,
31 =0.18, NS),the initial mean weight of spiderlings (FI,31=2.54, NS), or the final
mean weight of spiderlings (Fl,23 = 4.19, NS).Initial mean spiderling weights were
not different between with mother (mean= 2.2 1 f1.34 mg) and without mother
treatments (mean= 1.80 f0.86 mg) (b3= 0.88, NS).Similarly, final mean spiderling
weights were not different between with mother (mean=6.85 f4.2 1 mg) and without
mother treatments (mean= 4.38 f 1.80 mg) (k3=0.81, NS),although due to the low
survival of motherless spiderlings this may not be a meaningful result. Although I
observed only mothers attaching leaves onto the artificial nests a multiple regression
30
A
-
B
r
‘L
00
I
Group size
I
I)
Spiderling mass (mg)
Figure 4. Nest construction from the mother presence and spiderling number field experiment. The
number of leaves used in nest construction increases with A, increasing final group size, and B,
increasingfinal spiderling weights (multipleregression: r =0.66, y= 0.17 group size 3.30 weight - 3.25).
Groups with (m) and without (0)mothers; note that failed groups were not used in analysis (see text).
+
showed that final group size (Fig. 4A) and final mean weight (Fig. 4B) were correlated
with the number of leaves attached (r=0.66, F2,22 =8.43, R0.005).
In the laboratory experiment, all groups survived in the Drosophilu melanogaster
treatment because both mothers and spiderlings captured D. melanogaster. However,
only the mothers could capture Lucilia cuprina; consequently, groups without mothers
became cannibalistic after 2 weeks. Therefore, groups with mothers had higher
survival rate: 11 of the 12 groups with mothers persisted, compared with only 1
group without mothers (Fisher’s exact CO.00 1). The number of spiderlings that
survived the experiment depended on both the presence of the mother and prey
type (interaction Fl. 44=8.67, -0.01). Therefore the effect of the mother was
considered separately for each prey type. In the L. cuprina treatment, survival was
significantly higher with mothers (b2= 5.5 1, PCO.00 l), whereas in the D. melunogaster
treatment, spiderling survival was not affected by mother presence (hI2 = 1.17, NS)
(Fig. 5A).
Initial mean spiderling weight was not different between treatments (Fl,44 = 2.03,
NS), but final mean spiderling weights were different between treatments (Fl,20=
10.10, PC0.005, motherless L. cuprina treatment excluded due to low survival).
Motherless spiderlings fed D. melanogaster were significantly heavier than spiderlings
with mothers fed L. cuprina (ho= 3.18, -0.0 1). Otherwise, spiderlings with mothers
had similar final mean weights in both prey treatments (bo= 1.39, NS) and spiderlings
fed D. melanogaskr grew similar amounts with or without mothers (b2= 1.25, NS)
(Fig. 5B). Although mothers were of similar initial weight in both prey treatments
(h22 = 0.96, NS), mothers fed D. melanogaster did not change weight over the experiment
(paired k,=0.136, NS) whereas mothers fed L. cuprina increased in weight by 50%
(paired t5=2.89, -0.05) (Fig. 5C).
Retreats were made by binding the paper ‘leaves’ with silk, which also framed
the round entrances. The volume of retreat constructed depended on mother
presence (FI,+=14.8, P CO.001) and the prey type (Fl,44= 16.1, RO.OOl), and the
two effects were additive (interactionNS), as retreats built by groups without mothers
20
7-
a 15
^M 6 a
5 -
8
!d
1
1 4 -
I
3 10
M
i5
3
3 -
v)
s
v)
1 -
8 2-
0
40r
C
30
30bL
!I
!d
L
0
T
9
Q
x
T
20
ML?
20
MD2
Figure 5. Mother presence and prey size laboratory experiment. A, spiderling survival. B, growth of
spiderlings. C, mother weight change. D, size of retreat woven during the experiment. Initial (0)
and
weight. 0 =mother absent, M =mother present, L=Lucilia cuprina, D=L?msophilu melunogaster.
final (I)
Different numbers indicate significantly different values (see text).
fed D. melanogarter were the same as retreats built with mothers fed L. cuprina (h2=
0.09, NS) (Fig. 5D).
Efects ofgroup size
A total of 41 of the 52 groups persisted over the experiment. The proportion of
spiderlings that survived was affected by group size. A multiple regression shows
that initially larger groups (Fig. 6A) and initially heavier spiders (Fig. 6B) had
proportionately more surviving spiders (r=0.64, FL, 48 = 16.3, P<O.OOl). Those
groups which had attached leaves to their artificial nests endured the storm. The
number of attached leaves depended on the proportion of surviving spiders. A
multiple regression shows that larger groups (Fig. 6C) and heavier spiders (Fig. 6D)
had larger nests (r=0.72, F2,49=26.8, P<O.OOl).
Nests as pmtectiue retreats
The nest was crucial to the survival of the D. ergandms. All D. ergandms were eaten
by the C. mbusta in containers that did not contain a nest (ie. mortality of 100%).
I did not observe any active group defence by the D. ergandms against the C. mbusta,
SOCIAL CRAB SPIDERS
r
A
3
*>
9
0.8
’E
0.6
3e
0.4
&
9
*
.
.
215
..
..
...
B
0.2
0.0
0
20
40
60
Group size
0
5
10 15 20 25
Spider mass (mg)
Figure 6. Group size field experiment. The proportion of spiders surviving increased as a function of
A, final number of spiders in the group and B, final spider weight (multiple regression: r=0.64, y =
0.01 group size +0.04 weight-0.28). The size of the nest increased as a function of C, final number
of spiders in the group and D, final spider weight (multiple regression: r=0.72, y=0.51 group
size
+ 1.14 weight - 14.1) (see text).
indeed D.ergandros ignored other group members being eaten. However, 94.6% of
D. ergandros survived in containers with nests. The C. robusta made forays into the
artificial nests, but they were slowed due to the confined spaces, frequently chewing
through silk binding the ‘leaves’. The forays were always unsuccessful; D.ergandms
were never captured within their nests as they maintained distance and ‘leaves’
between themselves and the predator. The D.qandros repaired the damaged silk
connections once the C. robusta departed the nest. The D.qandros were vulnerable
when foraging on surface of the nest, which is when the C. mbusta made successful
captures.
DISCUSSI 0N
The care provided by Diaea ergandms mothers was shown in this study to be very
important in spiderling survival. Survey data showed that groups of D. qandros
began with mothers, who lived with their offspring over summer and provided the
bulk of the early nest construction. Mothers decreased in weight, perhaps due to
matriphagy and disappeared in the late autumn. The field and laboratory experiments
216
T. A. EVANS
demonstrated the importance of maternal nest construction and capture of large
prey, activities that spiderlings were unable to undertake. In the field experiment,
spiderlings without mothers dispersed, which suggested that remaining in a small
nest without a mother was more risky than dispersing. Spiderlings have been
observed to leave one nest and enter another, presumably to find a group with a
higher chance of success. Low survival without mothers may be due to (1) absence
of large prey items provided by mothers, (2) hungry siblings becoming cannibalistic
(Evans et al., 1995), or (3) a higher predation risk associated with smaller nests.
The permanent, expandable and protective nest built by D.qandms was shown
in this study to be very important in the survival of spiders also. Survey data showed
that nest size increased with group size and age; maximum nest size was attained
when spiders matured, also when predators were most common. The field experiment
demonstrated that larger nests were built by larger groups ofjuveniles and subadults,
but these bigger nests required less individual effort. These larger nests conferred
the highest level of spider survival. The nest provided defence against inclement
weather and predators. The small vertebrate predators that were able to sit on the
slender branchlets and leaves that support the nest were not able to penetrate larger
nests, whereas invading predacious spiders were foiled by its labyrinthine structure.
This was passive rather than active defence, yet it was communal defence because
nest construction and repair was performed by many individuals.
The two factors found in this study on D. qandms, i.e. parental care and a
permanent, expandable and protective retreat are common to other, diverse social
taxa, (Andersson, 1984; Alexander et ul., 1991; Seger, 1991). These factors are not
limited to thomisids among social spiders; indeed, all other social spiders exhibit
these characteristics as well (Shear, 1970; Burgess, 1976; Buskirk, 1981; D’Andrea,
1987; AvilCs, 1997). All social spiders, and closely related solitary and subsocial
species, exhibit some form of maternal care. Essential feeding either via regurgitation
or by prey provisioning occurs in the well studied social genera A g e h a (Agelenidae)
( K r f i , 1969; Darchen, 1973), StegodyPhus (Eresidae) (Kullman, 1972; Jacson &
Joseph, 1973; Seibt & Wickler, 1988; Schneider, 1995), Anelosimus (Theridiidae)
(Kullman, 1972; Brach, 1977; Christenson, 1984), Achuearunea (Theridiidae) (Lubin
& Robinson, 1982; Lubin, 1982). Scavenging prey remains may provide a similar
function, e.g. Dictynu and Mullos (Dictynidae) (Jackson, 1978, 1979), Budumna
(Amaurobiidae)(Gray, 1983; Downes, 1993)and Qrtophora (Araneida)(Lubin, 1974),
and Tapinillus (Oxyopidae) (Avilb, 1994). Matriphagy may also be important, as it
has been described from three social genera in Werent families: Diuea (Thomisidae)
(Evans et al., 1995); Stegodyphur (Eresidae)(Kullman, 1972; Kullman & Zimmerman,
1975; Seibt & Wickler, 1987; Schneider, 1995) and ’Iheridn and Anelosimus (Theridiidae) (Kullman, 1972; Brach, 1977).
All social spiders inhabit permanent, expandable and protective retreats; the most
common type is the snare web. All types of retreats are protective and are associated
with food supply, and so provide food as well as shelter. All social spider retreats, leaf
nests ( k a spp., Irapinillus sp., AvilCs, 1994), bark retreats (Delenu cuncdes, Rowell &
Avilks, 1995)or snare webs, can be enlarged as the group increases in size or needs. It
is interesting to note that the snare webs and retreats woven by non-territorial social
species appear to be analogous to multiple, combined exampleswoven by their solitary
relatives: e.g. Agelenidae ( K r f i , 1969; D’Andrea, 1987), Theridiidae (Brach, 1977;
Vollrath, 1982; Christenson, 1984; Lubin, 1986),Dictynidae (Jackson, 1978; Tietjen,
1986)and Eresidae (Seibt & Wickler, 1988; Schneider, 1995).
SOCIAL CRAB SPIDERS
217
There are no experimental studies that consider the importance of the snare web
to group survival in other social spider species. However, survey data have shown
that large groups make larger webs at lower individual cost for Anelosimus eximius
(Vollrath, 1982, 1986), Agehu consociutu (Riechert, Roeloffs & Echternacht, 1986),
Mullos gregulis (Tietjen, 1986), and Metepeiru spinipes F.O. Pickard-Cambridge (Uetz,
1986).As found for D. qundms, smaller groups or webs are more likely to go extinct
for Agelena consociutu (Riechert et ul., 1986; Roeloffs & Riechert, 1988), S.mimosarum
and S. dumicola (Seibt & Wickler, 1988), Anelosimus eximius (Vollrath, 1982; AvilCs,
1986; Venticinque, Fowler & Silva, 1993; Leborgne, Kraffit & Pasquet, 1994),
Achueurunea wuu (Lubin & Robinson, 1982), Metepeira spinipes (Uetz, 1986, 1988), and
M. incrussutu F.O. Pickard-Cambridge (Uetz & Hieber, 1994).
This study on D. ergandms and those of other social spiders support the universality
of parental care and permanent, expandable and protective retreats as important
factors that influence the evolution of social behaviour in all taxa (Andersson, 1984;
Alexander et ul., 1991; Seger, 1991). But questions remain to be answered. Maternal
care is nepotistic (Hamilton, 1987; Glutton-Brock, 1991), and social spiders groups
are kin based, yet social spiders have not yet been reported to have kin recognition.
Indeed, the lack of group closure distinguishes spider sociality from that found in
other taxa (Wilson, 197 1; Buskirk, 1981; Darchen & Delage-Darchen, 1986; Downes
1996).The influence and the adaptive value of these open groups, and the importance
of inclusive fitness (Hamilton, 1964a, b), if any, for the evolution and/or maintenance
of social behaviour in spiders, has yet to be examined experimentally for social
spiders. This group closure and inclusive fitness benefits may prove a fruitful area
of investigation offering new insights into the evolution of social behaviour in spiders.
ACKNOWLEDGEMENTS
My thanks to Emily Bolitho, Nathan Evans, and Sally Troy, for their help in the
field and laboratory, and to Mark Elgar, Robert Jackson, Michael Lenz, Michael
Magrath, Alain Pasquet and Nina Wedell for their discussion and comments that
improved this manuscript. Also, special thanks to Simon Ward for allowing me to
test nests with his Feather-tail gliders. I am grateful for the financial support provided
by the Australian Research Council, Ecological Society of Australia, Royal Society
of Victoria, Zoological Society of New South Wales, and the Department of Zoology,
University of Melbourne.
REFERENCES
Alexander RD, Noonan JM, Crespi BJ. 1991. The evolution of eusociality. In: Sherman PW,
Jarvis JUM, Alexander RD, eds. 'The biology ofthe naked mole rat. Princeton: Princeton University
Press, 3 4 4 .
Andersson M. 1984. The evolution of eusociality. Annual Review $Ecology and Systnnatics 15: 165-189.
Aviles L. 1986. Sex-ratio and possible group selection in the social spider Anelosimw eximiw. Ame7ican
Naturalid 128: 1-12.
AvilCs L, 1994. Social bchaviour in a web-building lynx spider, Tapinillus sp. (Araneae: Oxyopidae).
Biological3ournal dthe Linnean Soci-e~51: 163-1 76.
Aviles L. 1997. Causes and consequences of cooperation and permanent-sociality in spiders. In: Choe
-
218
T. A. EVANS
J, Crespi BJ, eds. Social competition and cooperation among insects and arachnids, II, evolution ofsocialig.
Cambridge: Cambridge University Press, 476498.
Brach V. 1977. Anelosimus studiosus (Araneae:Theridiidae)and the evolution of quasisociality in theridiid
spiders. Euolution 31: 154-161.
Bristowe WS. 1958. The WorM ofspiders. London: Collins.
BurgessJW. 1976. Social behaviour in group living spider species. Symposium ofthe /zoological Socieg of
London 42: 69-78.
Buskirk RE. 1981. Sociality in the Arachnida. In: Hermann H, ed. Social Insects (vol 2). New York:
Academic Press, 281-367.
Christenson TE. 1984. Behaviour of colonial and solitary spiders of the theridiid species Anelosimus
eximius. Animal Beharriour 32: 725-734.
Glutton-Brock TH.1991. 7he Evolution OfPamtal Care. Princeton: Princeton University Press.
Crespi BJ. 1992. Eusociality in Australian gall thrips. Nature 3 5 9 724-726.
D’Andrea M. 1987. Social behaviour in spiders (Arachnida Araneae). Monitore /zooh&o Ituliano, NS
Monograph 3.
Darchen R. 1973. Ecologie d’une araignke sociale (Agelena consociatu D.) a la lumikre de quelques
experiences de laboratoire. Insectes Sociaux 20: 379-384.
Darchen R, Delage-Darchen B. 1986. Societies of spiders compared to the societies of insects.
30~rnalofdrachnology 14: 227-238.
Darwin C. 1845. A naturalist’s myage: Joumal of researches into the natural histoy of geology of the countries
visited during the vvage ofthe H M S Beagle mund the worM, under the command of Capt. Fitzmy, RN.London:
John Murray, 1897 edn.
Downes ME 1993. The life history of Badumm candida (Araneae: Amaurobioidea).Australian Journal
of/zoohgy 41: 441466.
Downes MF. 1996. Australasian social spiders: what is meant by ‘social’? Records ofthe W e s h Australian
Museum, S u p p h m t 52: 15 1-1 58.
D u e JE. 1996. Eusociality in a coral-reef shrimp. Nature 381: 512-5 14.
Evans TA. 1995. Two new social crab spiders (Thomisidae: D k a ) from eastern Australia, their
natural history and geographic range. Reconh ofthe W e s h Australion Museum, S u p p h m t 52: 151-158.
Evans TA. 1997. Distribution of social crab spiders in eucalypt forests. AuttralianJoumal ofEcology 22:
107-1 11.
Evans TA, Main BY. 1993. Attraction between social crab spiders: evidence of pheromonal
communication in Diaea socialis (Thomisidae). Behavioural Ecology 4 99-1 05.
Evans TA, Wallis FJ, Elgar MA. 1995. Making a meal of mother. Nature 376: 299.
Gray MR. 1983. The taxonomy of the semi-communal spiders commonly referred to as the species
Ixeuticus candidus (L. Koch) with notes on the genera Phryganoporus, Ixeuticus and Badumna (Araneae,
Amaurobiidae). Pmceedings of the Linnean So&& ofNS. W 106: 247-26 1.
Hamilton WD. 1964a, b. The genetical evolution of social behaviour I & 11. Journal of 7lzeoetical
Biohgy 7: 1-52.
Hamilton WD. 1987. Discriminating nepotism: expectable, common, overlooked. In: Fletcher DJC,
Michener CD, eds. f i n recognition in animals. New York J. Wiley & Sons, 417437.
Jackson RR. 1978. Comparative studies of Dicwa and Mallos (Araneae, Dictynidae) I. Social
organisation and web characteristics. Revue Arachnologique 1: 133-164.
Jackson RR. 1979. Predatory behaviour of the social spider Mallos gregalis is it cooperative? Insectes
S o c i a ~26:
~ 300-3 12.
Jacson CC, Joseph KJ. 1973. Life-history bionomics and behaviour of the social Stegodyphus sarasinorum
Karsh. Insectes S O C ~ ~20:
U X189-204.
Kr& B. 1969. Various aspects of the biology of Agelena consociatu Denis when bred in the laboratory.
A d a n /zoologist 9: 20 1-2 10.
Kullmann EJ. 1972. Evolution of social behaviour in spiders (Araneae; Eresidae and Theridiidae).
Amenkan /zoohgist 12: 419-426.
Kullman FJ, Zimmerman W. 1975. Regurgitationsfutterungen als bestandteil der brutftirsorge bei
haubennetz und rohrenspinnen (Araneae, Theridiidae und Eresidae).Pmceedings ofthe 6th International
Arachnological Congress (1974), 120-1 24.
Leborgne R, KrafFt B, Pasquet A. 1994. Experimental study of foundation and development of
Anelosimus eximius colonies in the tropical forest of French Guiana. Insectes Sociaux 41: 179-189.
Lubin YD. 1974. Adaptive advantages and the evolution of colony formation in Cyrtophora (Araneae:
Araneidae). ~001ogicalJoumalofthe Linnean Socieg 54: 32 1-339.
SOCIAL CRAB SPIDERS
219
Lubin YD. 1982. Does the social spider Achaearanea wau (Theridiidae) feed its young? ZeitschnJfitr
lierpsycholoffie 60: 127-1 34.
Lubin-iTI. 1986. Courtship and alternative mating tactics in a social spider. Journal ofArachnology 14:
239-257.
Lubin YD,Robinson MH. 1982. Dispersal by swarming in a social spider. Science 216: 3 19-32 1.
Main BY. 1988. The biology of a social thomisid spider. In: Austin AD, Heather NW, eds. Australian
Arachnologv. Brisbane: Australian Entomological Society Miscellaneous Publication #5, 55-73.
Riechert SE, Roeloffs R, Echternacht AC. 1986. The ecology of the cooperative spider Agelena
consociata in equatorial Africa (Araneae, Agelenidae).Journal ofArachnology 1 4 175-1 92.
Roeloffs R, Riechert SE. 1988. Dispersal and population-geneticstructure of the cooperative spider,
Agelma consociata, in west African rainforest. Evolution 42: 173- 183.
Rowell DR, Avilks L. 1995. Sociality in a bark-dwelling huntsman spider from Australia, Delena
cancerides Walckenaer (Araneae: Sparassidae). In-sectes Sociaux 42: 287-302.
Rypstra AL. 1993. Prey size, social competition and the development of reproductive division of
labor in a social spider group. American Naturalist 142: 868-880.
Schneider JM. 1995. Survival and growth in groups of a subsocial spider (Stegodyphus lineah). Imectes
Sociaux 42: 237-248.
Seger J. 1991. Cooperation and conflict in social insects. In: Krebs JR, Davies NB eds. Behavioural
ecology (3rd ed). Oxford: Blackwell Scientific Publications, 338-373.
Seger J, Moran NA. 1996. Snapping social swimmers. Nature 381: 473-474.
Seibt U, Wickler W.1987. Gerontophagy versus cannibalism in the social spider Stego&phus mimosarum
Pavesi and Stego@hus dumicola Pocock. Animal Behaviour 35: 1903-1 905.
Seibt U, Wickler W.1988. Bionomics and social structure of 'Family Spiders' of the genus Stegodyphus
with special reference to the African species S.dumicola and S.mimosarum (Araneida, Eresidae). Verh.
naturwiss. Va Hamburg 30: 255-303.
Shear WA. 1970. The evolution of social phenomena in spiders. Bulletin of the British Arachnological
Sociep 1: 65-75.
Sokal RR, Rohlf FJ. 1981. Biomety, 2nd edn. New York: WH Freeman and Co.
Tietjen WJ.1986. Effects of colony size on web structure and behaviour of the social spider Mallos
gregalis (Araneae, Dictynidae).Journal of Arachnology 14: 145-157.
Uetz GW. 1986. Web building and prey capture in communal orb weavers. In: Shear WA, ed. Spiders:
webs, behaviour and evolution. Stanford: Stanford University Press, 207-23 1.
Uetz GW.1988. Risk sensitivity and foraging in colonial spiders. In: SlobodchikoffCN, ed. 7?zeecology
ofsocial behaviour. New York Academic Press, 353-377.
Uetz GW,Hieber CS. 1994. Group size and predation risk in colonial web building spiders: analysis
of attack abatement mechanisms. Behauioural Ecology 5: 326-333.
Vollrath F. 1982. Colony foundation in a social spider. &tschriJfitr Trn~ychologit60: 3 13-324.
Vollrath F. 1986. Environment, reproduction and the sex ratio of the social spider Anelosimus eximius
(Araneae, Theridiidae).Journal ofArachnology 1 4 267-281.
Venticinque EM, Fowler HG, Silva CA. 1993. Modes and frequencies of colonisation and its
relation to extinctions, habitat and seasonality in the social spider Anelosimus in the amazon
(Araneidae:Theridiidae). Pyche 100: 3541.
Wilson EO. 1971. 7?ie insect societies. Cambridge Mass.: Harvard University Press.