Natal Dispersal Patterns of a Subsocial Spider
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Ethology 109, 725—737 (2003)
2003 Blackwell Verlag, Berlin
ISSN 0179–1613
Natal Dispersal Patterns of a Subsocial Spider
Anelosimus cf. jucundus (Theridiidae)
Kimberly S. Powers & Leticia Avilés*
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson,
AZ, USA
Abstract
Species that alternate periods of solitary and social living may provide clues
to the conditions that favor sociality. Social spiders probably originated from
subsocial-like ancestors, species in which siblings remain together for part of their
life cycle but disperse prior to mating. Exploring the factors that lead to dispersal
in subsocial species, but allow the development of large multigenerational
colonies in social species, may provide insight into this transition. We studied the
natal dispersal patterns of a subsocial spider, Anelosimus cf. jucundus, in
Southeastern Arizona. In this population, spiders disperse from their natal nests
in their penultimate and antepenultimate instars over a 3-mo period. We tracked
the natal dispersal of marked spiders at sites with clustered vs. isolated nests. We
found that most spiders initially dispersed less than 5 m from their natal nests.
Males and females, and spiders in patches with different densities of nests,
dispersed similar distances. The fact that both sexes in a group dispersed, the lack
of a sex difference in dispersal distance, and the relatively short distances
dispersed are consistent with the hypothesis that natal dispersal results from
resource competition within the natal nest, rather than inbreeding avoidance in
competition for mates. Additionally, an increase in the average distance dispersed
with time and with the number of spiders leaving a nest suggests that competition
for nest sites in the vicinity of the natal nest may affect dispersal distances. The
similar distances dispersed in patches with isolated vs. clustered nests, in contrast,
suggest that competition among dispersers from different nests may not affect
dispersal distances.
Corresponding author: Kimberly S. Powers, Department of Ecology
and Evolutionary Biology, University of Arizona, 1041 E. Lowell St, Tucson,
AZ 85721, USA. E-mail: kspowers@email.arizona.edu
*Present address: Leticia Avilés, Department of Zoology, University of
British Columbia, BC Canada V6T 1Z4, Canada.
U. S. Copyright Clearance Center Code Statement: 0179-1613/2003/1099–0725/$15.00/0 www.blackwell.de/synergy726 K. S. Powers & L. Avilés
Introduction
Across taxonomic systems, periods of communal living are frequently offset
by dispersal events followed by solitary living (see Waser & Jones 1983; Tallamy
& Wood 1986; and Plateaux-Quénu et al. 1997 for examples in mammals and
insects). Understanding the factors responsible for such dispersal events should
offer insight into the conditions that cause animals to live communally vs.
solitarily. Subsocial spiders (Buskirk 1981; Avilés 1997) are one system in which
individuals alternate periods of communal and solitary living. In such species,
clutchmates remain together within their natal nest and cooperate in web
building, prey capture, and feeding. These cooperative behaviors diminish as
spiders approach reproductive maturity. One to several instars before maturity,
they leave the natal nest and become solitary. Solitary females then raise their
offspring independently. In contrast, social spider (Buskirk 1981; Avilés 1997)
nestmates remain together throughout their lives, mate and reproduce within their
natal nests, and aid each other in raising offspring. These differences translate into
different breeding structures: while the subsocial species appear primarily outbred,
most social species are highly inbred, forming colonies that develop into
reproductively isolated lineages with low genetic variability and female-biased
sex ratios (Avilés 1986, 1993, 1997; Vollrath 1986; Roeloffs & Riechert 1988).
Several lines of evidence suggest that social spiders originated from subsocial-like
ancestors, a transition that would have involved suppression of the dispersal
phase (Kullmann 1972; Krafft 1979; Ruttan 1990; Gundermann et al. 1993;
Wickler & Seibt 1993; Schneider 1995; Avilés 1997). To understand this
transition, we must explore the factors that lead to dispersal in the subsocial
species, but allow the development of large multigenerational colonies in social
species.
Resource competition, mate competition, and inbreeding avoidance have been
proposed as three major causes of natal dispersal (reviewed in Johnson & Gaines
1990). The resource competition hypothesis conjectures that siblings disperse in
order to avoid competing with each other for resources in resource-limited habitats
(Hamilton & May 1977) and predicts that males and females disperse with equal
probability when they have similar resource requirements (Motro 1991; Negro
et al. 1997; Gandon 1999; Perrin & Mazalov 2000; but see Forero et al. 2002). The
mate competition hypothesis suggests that individuals disperse to avoid competing
with siblings for mates and predicts that the sex suffering the highest cost from
intrasexual mate competition will disperse farther (Greenwood 1980; Dobson
1982; Moore & Ali 1984). Given that only females care for offspring in subsocial
spiders, males should be more likely to compete for mates than females, according
to standard sexual selection theory. The inbreeding avoidance hypothesis suggests
that individuals disperse away from their natal site to avoid mating with relatives
and also predicts sex-biased dispersal (Greenwood 1980; Cockburn et al. 1985;
Motro 1991; Gandon 1999; Perrin & Mazalov 1999). According to Waser et al.
(1986), the sex likely to suffer greater fitness costs by forfeiting inbred matings –
usually the sex with fewer mating opportunities on average – should disperseNatal Dispersal Patterns of a Subsocial Spider 727
farther. According to Perrin & Mazalov (1999), males should be the dispersing sex
if females prefer immigrant males. Thus, while a sex bias in either direction could
support the mate competition and inbreeding hypotheses, the lack of a sex bias is
only consistent with the resource competition hypothesis.
Following or during dispersal, siblings may still compete for nest sites or
resources. Such competition would be reflected in greater dispersal distances when
the number of dispersing siblings is greater and over time as nearby sites become
occupied. Spiders may also compete with individuals dispersing from neighboring
nests within their local area. Greater dispersal distances would then be predicted
for spiders dispersing in sites with greater densities of nests. Alternatively, if
inbreeding avoidance is the primary factor affecting dispersal distances, longer
distances are predicted for spiders dispersing out of sites with lower densities of
nests, where outcrossing opportunities are more limited.
In order to gain insight into the factors responsible for dispersal in subsocial
spiders, we investigated the natal dispersal patterns of Anelosimus cf. jucundus (see
below) in southern Arizona. Avilés & Gelsey (1998) found that individuals of this
species typically disperse short distances from their parental nests prior to
becoming adults and that colonies are patchily distributed. However, because they
did not mark individual spiders, Avilés & Gelsey (1998) could only estimate
dispersal distances from single, isolated nests. Using marked individuals
dispersing from nests in patches of two discrete densities of nests, we investigated
dispersal distances in relation to dispersal timing, disperser sex, and local density
of nests. We examine our findings in light of the three hypotheses proposed to
explain dispersal.
Methods
Study Species
Anelosimus cf. jucundus is morphologically close, but not identical to
Anelosimus jucundus (O. P. Cambridge 1986), a subsocial species described from
montane areas in Costa Rica, Panama, and Ecuador (Levi 1956, 1963; I. Agnarsson
pers. comm.). The life history and phenology of A. cf. jucundus in sourthern Arizona
has been described in detail by Avilés & Gelsey (1998); see also Bukowski & Avilés
2002). Nests are basket-shaped tangle webs built at the ends of branches and
distributed singly or in clusters of up to a few dozen. New nests are established
during the dispersal season (May–early August) when subadult to young adult
males and females abandon their natal nests to continue their growth and
maturation in individual nests. Following a brief mating period (late July–early
August) during which males typically visit females in their webs, females lay a single
egg sac containing an average of 35 eggs (range 21–53, Avilés & Gelsey 1998).
Mothers care for their offspring through early December; by this time, most mothers
have died or (less often) been eaten by their offspring. Siblings continue to coexist
within their natal nest until the following dispersal season. During the period of
coexistence, siblings cooperate in prey capture and share their food.728 K. S. Powers & L. Avilés
We conducted the study over two dispersal seasons – 1998 and 2002 – at the
Patagonia-Sonoita Creek Preserve (3130¢N, 11050¢W, 1500 m) where
A. cf. jucundus nests are distributed within approximately 25 m of a creek. Each
year, we collected nests from the field 1–3 wk prior to the onset of the dispersal
season. We brought the nests to the laboratory where we disassembled them to
count and, in some cases (see below), mark the spiders they contained. We
returned the nests to the field where we reassembled them by combining original
nest materials and nestmates in a hairnet and fastening them to a branch. The
spiders rebuilt the nest within a day of their return. Our methodology allowed us
to detect individuals dispersing immediately following, possibly as a result of the
procedure. These individuals (n ¼ 3 in 1998) were excluded from the analyses. As
a control (see below), we also included nests that we had not disassembled (1998
and 2002) or relocated (1998). We marked the spiders with fast-drying acrylic
paint, using the same color for nestmates and different colors for spiders
belonging to different colonies in the same patch (one or two small paint dots on
the dorsal side of the abdomen). Spiders were in their fourth and fifth instars when
marked (instars as defined in Avilés & Gelsey 1998). Dispersal distances for
marked spiders are for these instars only, as individuals that molted prior to
dispersal would have lost their mark.
Experimental Design
During the 1998 dispersal season, we examined dispersal timing and distance
of males and females in nest patches of two densities: single, isolated nests and
multiple, clustered nests (Fig. 1). Isolated nests (n ¼ 15) were separated from any
other nest by at least 20 m. We artificially isolated 10 of these nests by removing
them from their original site and relocating them to sites resembling typical nest
sites in vegetation type and amount and height of foliage. To represent clustered
nests, we included three nests in each of two patches containing 10 and 20 mature
nests and four nests in a patch containing 45 mature nests. Nearest neighbor
distances among mature nests in a patch ranged from 0.1 to 7.2 m
(median ¼ 0.9 m; estimated by Avilés & Gelsey 1998). The three clustered
patches were separated from each another by approximately 0.4–0.5 km.
Also during the 1998 dispersal season, we marked all spiders from clustered
nests and from seven of the artificially isolated nests to identify dispersersÕ natal
nests. We left spiders unmarked in three artificially isolated nests to control for
any effect of nest disassembly and marking. Four naturally isolated nests were
also left untouched to control for any effect of nest relocation. Each isolated nest
thus belonged to one of three treatment categories (Fig. 1): (1) naturally isolated,
unmarked, (2) artificially isolated, unmarked, (3) artificially isolated, marked.
With this design, any effect of nest relocation could be detected by comparing
dispersal distances between groups (1) and (2). Effects of nest relocation, nest
disassembly, and spider marking would be revealed by comparing dispersal
distances between groups (1) and (3).Natal Dispersal Patterns of a Subsocial Spider 729
Local site type (1998) Nest density site of origin (2002)
Isolated Clustered High Low
Disassembled
Naturally isolated, Four nests Yes Eight nests Nine nests
unmarked
Artificially isolated, Three nests
No Seven nests Five nests
unmarked
Artificially isolated,
disassembled/ Seven nests 10 nests
(Three sites)
marked
Fig. 1: Schematic representation of the experimental design showing the number of nests per category
that yielded dispersers. All 2002 nests were relocated and artificially isolated. Half of the spiders in each
of the 2002 disassembled nests were marked
Because our 1998 experimental design did not account for potential effects of
density of nests at their site of origin (all nests at clustered sites had originated
within those sites), we conducted a second experiment in 2002 in which we
established 40 isolated nests, half originating at high density locations (clustered
conditions) and half at low density locations (isolated conditions). To further test
for manipulation effects, we disassembled half of the nests in each category and
marked half of the spiders each contained; we relocated the other nests without
disassembling them. We marked only half of the spiders in each nest to distinguish
between the separate effects of disassembling nests and marking spiders. We
organized nests into groups of four, with one nest of each category per group. We
then established these nests in the field, making sure that they were isolated from
others by at least 20 m. Twenty nine out of the forty original nests yielded
dispensers (Fig. 1).
We measured dispersal distances from new, solitary webs to spidersÕ natal
nests, either the sole nest at isolated sites (with marked or unmarked spiders) or
the nest matching the color of a spider’s mark at clustered sites. We surveyed each
site for new, solitary webs containing dispersed individuals once every 2 wk from
May 17 to August 22, during the 1998 season, and once a week from May 31 to
September 1, during the 2002 season. We continued to examine previously
discovered solitary webs for new residents, inferred by a difference in mark, sex,
and/or instar. When new residents were found (n ¼ 22 in the 1998 season and
n ¼ 4 in 2002), we recorded their dispersal distance as a new dispersal event.
When making inferences based on age differences, we did not consider an increase
by one instar to indicate the presence of a new resident.
Data Analysis
In our analyses, we include natal nest identity (nest ID) as a random effect
nested within treatments that were relevant to whole nests, i.e. whether the nests
were disassembled or not (both years), local nest density (1998), and nest density
in the area of origin (2002). Factors that were properties of individuals, such as730 K. S. Powers & L. Avilés
sex and instar, were nested within nest ID. We considered a few individuals who
remained within 6 cm of their natal nests (n ¼ 5 in 1998 and n ¼ 11 in 2002, see
results) to not have dispersed and excluded them from the analyses. Additionally,
in 1998 we excluded one long distance outlier (fourteen standard deviations above
the mean) of uncertain origin. We also excluded three individuals who abandoned
their nest immediately upon nest re-establishment because our experimental
manipulation seemed to have provoked their dispersal. For all analyses, we
natural log transformed dispersal distance and timing. When reporting central
tendencies of dispersal distances, we have used median values. Mean values are
reported with ± standard error.
Experimental Manipulation Effects
Comparing the three categories of isolated nests in 1998 (Fig. 1), we found
no effect of nest relocation on dispersal timing (t12.6 ¼ 1.75, p ¼ 0.11) or on
dispersal distance (t14.2 ¼ )1.54, p ¼ 0.14, for the contrast between treatments 1
and 2 in a model including nest ID as a random effect nested within treatments, as
discussed in above). Thus, in all of our 1998 analyses we have combined data from
these two treatments. In 1998, we also found no significant effect of nest
disassembly relocation plus on dispersal timing (t12.6 ¼ 1.39, p ¼ 0.19) or
dispersal distance (t14.2 ¼ 0.15, p ¼ 0.88, for the contrast between treatments 1
and 3, same model as above). Likewise, in 2002 we found no significant effect of
nest disassembly on dispersal timing (F1,35.5 ¼ 0.59, p ¼ 0.45, R2 ¼ 0.61) or
distance (F1,35.5 ¼ 0.96, p ¼ 0.33, R2 ¼ 0.62) in a fully factorial model that
included nest ID as a random factor nested within the four categories resulting
from the cross of nest disassembly and density of nests (clustered vs. isolated) at
the site of origin. We thus combined the data for disassembled and non-
disassembled nests in all our analyses. Because of the small number of marked
spiders recovered in 2002 (see below), we were unable to test for the effect of
marking the spiders per se on dispersal distance and timing.
Results
In 1998, we obtained complete dispersal distance and timing information for
140 spiders (60 marked) dispersing from 17 dissassembled and eight non-
disassembled nests. In 2002, we obtained similar information for 70 spiders (nine
marked) dispersing from 17 disassembled and 12 non-disassembled nests.
Disassembled nests contained an average of 22.4 ± 1.96 spiders (n ¼ 27 nests)
in 1998 and 12.5 ± 1.29 spiders (n ¼ 24 nests) in 2002 (the large difference in
number of spiders per nest between years was probably because of the severe
Arizona drought of 2002). Dispersal distances ranged from 15 to 504 cm
x ¼ 86 cm; n ¼ 105 spiders from isolated sites only) in 1998 and from 7 to
(~
926 cm (~x ¼ 124 cm; n ¼ 70) in 2002 (Fig. 2). All marked dispersers that we
recovered possessed a mark that matched a color from a colony within their site,
suggesting that successful dispersal across sites did not occur at this stage.Natal Dispersal Patterns of a Subsocial Spider 731
40
1998
35
2002
30
Number of spiders
25
20
15
10
5
0
0–50
51–100
101–150
151–200
201–250
251–300
301–350
351–400
401–450
451–500
501–550
Dispersal distance (cm)
Fig. 2: Distribution of dispersal distances during 1998 (n ¼ 105 spiders from isolated nest sites only,
outliers excluded) and 2002 (n ¼ 70) dispersal seasons. Seven spiders that in 2002 dispersed >550 cm
not shown, but included in the analyses
Distances between naturally occurring neighboring sites in 1998 ranged from 29
to 195 m, with an average of 76.9 ± 10.7 m (n ¼ 18 sites).
In both years, we found a significant increase in dispersal distances with time
(Fig. 3). Type I sum of squares (SS) of a model with nest ID as a random effect
nested within site-type categories (isolated vs. clustered, either under current local
conditions in 1998 or in the area where nests originated in 2002) showed that
7 7 •
• •
•• • •
• •• • • •••
6 •• •• •• 6 •
•• • • •
ln distance (cm)
ln distance (cm)
•
•
• • •• •• •• •
• ••• •• •• •
5 • ••••• ••••• •• •
•
• • • 5 • • •• •• • •
• ••• • • • • •
•• •
•• • • • •
•• •• •••• • •• • • •• •
4 • •• ••••• ••
• •• • 4 • • •• • •
• • •• • • • •
• ••• •••
••• •• • • • •• •
• • • •
3 • • • 3 • •
• ••
• •• • • • •
• •
•
2 2 •
• •
1998 2002
1 1
2.5 3 3.5 4 4.5 5 2 2.5 3 3.5 4 4.5
ln number of days ln number of days
Fig. 3: Increase in dispersal distance over time (1998: n ¼ 140, isolated and clustered sites included;
2002: n ¼ 70). Outliers (see methods) excluded both years732 K. S. Powers & L. Avilés
dispersal timing explained a significant fraction of the variance both years – 9.7%
in 1998 (F1,115 ¼ 20.2, p < 0.0001, R2 ¼ 0.45) and 23.9% in 2002 (F1,42 ¼ 31.6,
p < 0.0001, R2 ¼ 0.68; timing, site type, and nest ID introduced in that order).
Not surprisingly, a spider’s dispersal timing strongly correlated with its instar
(Pearson correlation coefficient, r ¼ 0.73, p < 0.0001, 1998 data, all nests
included, with instar treated as a continuous variable), such that later dispersers
belonged to larger instars. In our analyses we use timing as a covariate, rather
than instar, because we had a more complete data set for this variable.
We examined whether there were sex differences in dispersal distance between
males and females by adding to these models sex as a factor nested within nest ID
and calculating standard Type II SS. We found no significant difference in
dispersal distance between the sexes in 1998 (F20,85 ¼ 1.35, p ¼ 0.18, R2 ¼ 0.55;
same data as above, but excluding 14 spiders whose sex could not be determined;
n ¼ 126; power ¼ 0.80) or in 2002 (F7,17 ¼ 1.3, p ¼ 0.30, R2 ¼ 0.84; excluding
spiders whose sex could not be determined; n ¼ 44, power ¼ 0.41).
We examined the hypothesis that competition among nestmates influences
their dispersal distance by comparing the average distances dispersed across nests
with different numbers of spiders. Based on this hypothesis, we predicted that
spiders from nests containing more spiders should disperse greater distances. Our
data supported this hypothesis (F1,5 ¼ 8.76, p ¼ 0.03, R2 ¼ 0.64, for a least
squares regression of the average distance dispersed from nests of different size
classes in 1998; Fig. 4).
On the other hand, we found no significant effect of local nest density on
dispersal distance when comparing spiders found marked at isolated vs. clustered
5.00
4.75
ln mean distance (cm)
4.50
4.25
4.00
3.75
3.50
0 1 2 3 4 5
Nest size class
(ln mean no. dispersers per nest)
Fig. 4: Mean dispersal distance increases with the total number of individuals dispersing from a nest
(n ¼ 151 spiders that dispersed in 1998, including 11 spiders for whom dispersal timing was not
determined; outliers excluded)Natal Dispersal Patterns of a Subsocial Spider 733
sites (we restrict our analysis to marked spiders as late dispersers that had lost
their mark could not be identified at clustered sites). Marked spiders recovered in
1998 dispersed 38 cm (~ x; n ¼ 18) at isolated sites and 48 cm (~x; n ¼ 42) at
clustered sites (F1,24.1 ¼ 0.06, p ¼ 0.81, R2 ¼ 0.60; timing, site type, and nest ID
in the model, excluding one outlier at the isolated sites). In 2002, we tested
whether the density of nests at their site of origin influenced dispersal distance and
found no significant effect (F1,38.5 ¼ 0.7, p ¼ 0.80, R2 ¼ 0.68). The latter two
results, however, should be taken with caution as the power of both tests was low
(power ¼ 0.06, LSV ¼ 1.3 m both years).
Discussion
Consistent with the resource competition hypothesis, but not with the mate
competition or inbreeding avoidance hypotheses (Dobson 1982; Waser et al.
1986; Motro 1991; Byrom & Krebs 1999; Gandon 1999; Perrin & Mazalov 1999,
2000; see also review in Johnson & Gaines 1990), we found no asymmetry in
dispersal distances between A. cf. jucundus males and females. Perrin & Mazalov
(1999) have argued that Ôcases in which both sexes disperse cannot be explained
solely by inbreeding avoidanceÕ (p. 289). Additionally, the short distances that the
spiders dispersed – a ~ x of 86 cm in 1998 and 124 cm in 2002 – appear clearly
insufficient to prevent sibling encounters at isolated nest sites and would have
allowed mixing of spiders from only the most immediate neighboring nests at
clustered sites. Given similarly short dispersal distances in previous generations, in
the latter case the possibility of inbreeding would still be open because members of
neighboring nests would still be somewhat related. Comparably short dispersal
distances have been reported for another subsocial spider, Stegodyphus lineatus
(Lubin et al. 1998; Johannesen & Lubin 2001).
Several lines of evidence support resource competition as the primary cause
of natal dispersal in subsocial spiders. Jones & Parker (2000) found that per
individual prey capture decreased with colony size in the subsocial spider
Anelosimus studiosus. In separate studies in A. cf. jucundus, we have found that
pre-dispersal body size is inversely related to clutch size (Aviles, Bukowski, &
Kenyon, unpubl. data) and that most of the growth in spider body size occurs
after dispersal (Avilés & Gelsey 1998). Furthermore, several researchers have
succeeded in prolonging the group-living phase in subsocial species by
supplementing colonies with food (Krafft et al. 1986; Ruttan 1990; Gundermann
et al. 1993; Schneider 1995; Kim 2000; see also Rypstra 1986; Evans 1998).
The geographic distribution of sociality in spiders is consistent with these
observations. While social species occur solely in tropical or subtropical regions
(Levi 1956, 1963; Avilés 1997; but see Furey 1998) where prey tend to be larger
(Schoener & Janzen 1968; Barlow 1994; Hawkins & Lawton 1995) and maintain
higher abundances throughout the year (MacArthur 1972; Janzen 1973; Young
1982), subsocial species occur predominantly in temperate regions or the
highlands of tropical regions where prey are expected to be smaller and less
abundant. Thus, social spiders probably experience an overall greater prey734 K. S. Powers & L. Avilés
biomass in lowland tropical and subtropical areas, allowing them to delay
dispersal and reach much larger colony sizes.
There are at least three non-mutually exclusive hypotheses to explain the
observed pattern of increased dispersal distance with time (Fig. 3): (a) later
dispersers traveled farther simply because of their larger size, (b) they traveled
farther because nearby sites were already occupied, and (c) spiders in nearby
newly-established nests were forced to relocate to greater distances after being
displaced by later dispersers. J. Moya-Laraña (pers. comm.) found that in the
congeneric Anelosimus vittatus the speed of displacement along silk strands is
positively correlated with spider body size. Traveling at a faster rate may allow
larger spiders to reach farther distances before settling.
Support for the hypothesis that competition for nest sites in the vicinity of the
natal nest may affect dispersal distance comes from the observation that average
dispersal distances were greater when the number of spiders dispersing from a nest
was greater (Fig. 4). Likewise, the left skewed distribution of dispersal distances
(Fig. 2) is consistent with a model in which individuals disperse more or less in a
straight line to the first available site, traveling longer distances when nearby sites
are already occupied (see Tonkyn & Plissner 1991), rather than searching
exhaustively all sites closest to the natal nest before moving further out (Murray
1967; Waser 1985; Buechner 1987; Tonkyn & Plissner 1991). Arguing against
sibling competition as the sole explanation for increased dispersal distance with
time is the fact that the pattern was also present in 2002 when very few spiders
dispersed from individual nests.
Lastly, competitively dominant dispersers may displace the residents of
newly-established webs, forcing them to disperse again (sensu Vollrath 1987). In
1998, we recorded 22 cases of dispersing spiders moving into newly-established
webs built by previous residents. Of these, it is not clear whether previous
residents were displaced or had previously abandoned their nest, perhaps as a
result of poor local conditions. It has been shown that spiders may experience
greater environmental variation in prey capture success when foraging solitarily
than when foraging in groups (Rypstra 1989; Caraco et al. 1995; Jones & Parker
2000, 2002). Relocating within patches may be one way to cope with such
variation (Vollrath 1987; Ward & Lubin 1993).
The short distances dispersed relative to the median distance among mature
nests in a cluster (90 cm) suggests that interactions among spiders dispersing from
different nests may not greatly influence dispersal distances, in particular if one
considers that the three-dimensional space surrounding a nest increases to the
third power as a disperser moves away from it. The absence of a difference in
dispersal distances at clustered vs. isolated sites further suggests absence of
competition among spiders dispersing from different natal nests, although this
result remains somewhat inconclusive because of the reduced sample of marked
spiders recovered.
We suggest that natal dispersal in this species primarily reflects competition
for resources within the natal nest and that inbreeding avoidance, if present, is
accomplished through alternative mean such as differences in maturation datesNatal Dispersal Patterns of a Subsocial Spider 735
between sibling males and females combined with later movements of one or both
sexes (Bukowski & Avilés 2002). Anelosimus cf. jucundus females mature after
males and only become sexually receptive 10 d after maturation (Bukowski &
Avilés 2002). This timing asymmetry may provide males the time needed to access
reproductively mature females in foreign sites during breeding dispersal (sensu
Greenwood 1980; Johnson 1986).
We should note that our focus on the forces responsible for natal dispersal in
subsocial and social spiders (i.e. what causes the disintegration of their social
groups) leaves open the question of why they live in groups in the first place.
Factors as varied as predator protection (e.g., Henschel 1998), access to prey too
large for individual spiders to capture (e.g., Pasquet & Krafft 1992), reduced per
capita investment in silk (Riechert 1985), thermal control (Seibt & Wickler 1990),
and presence of surrogate caregivers in the event of the mother’s death (TJ Jones
& S. Riechert, pers. comm.) have all been suggested to promote group living in the
more derived social species (reviewed in Avilés 1997). The factors responsible for
sibling coexistence following the period of maternal care in the subsocial species
have received less attention, but are likely to be similar to those suggested for the
social species. In general, we suspect that while the factor (or factors) primarily
responsible for group living in any one case may be highly idiosyncratic to the
particular species and the environment it occupies, resource limitation may turn
out to be universally responsible for the disintegration of social groups and, thus,
for setting a limit to group size and level of sociality across spider taxa.
Acknowledgements
We thank Jeff Cochrane for field assistance during the 2002 dispersal season and Asher Cutter,
Todd Bukowski, and three anonymous reviewers for comments on the manuscript. This research was
supported by NSF Grant DEB-9815938 to LA.
Literature Cited
Avilés, L. 1986: Sex ratio bias and possible group selection in the social spider Anelosimus eximius. Am.
Nat. 128, 1—12.
Avilés, L. 1993: Newly discovered sociality in the neotropical spider Aebutina binotata. J. Arachnol. 21,
184—193.
Avilés, L. 1997: Causes and consequences of cooperation and permanent-sociality in spiders. In: Social
Behavior in Insects and Arachnids (Choe, J. C. & Crespi, B. J., eds). Cambridge University Press,
New York. pp. 476—498.
Avilés, L. & Gelsey, G. 1998: Natal dispersal and demography of a subsocial Anelosimus species and its
implications for the evolution of sociality in spiders. Can. J. Zoolog. 76, 2137—2147.
Barlow, N. D. 1994: Size distributions of butterfly species and the effect of latitude on species size.
Oikos 71, 326—332.
Buechner, M. 1987: A geometric model of vertebrate dispersal: tests and implications. Ecology 68,
310—318.
Bukowski, T. C. & Avilés, L. 2002: Asynchronous maturation of the sexes may limit close inbreeding in
a subsocial spider. Can. J. Zool. 80, 193—198.
Buskirk, R. E. 1981: Sociality in the Arachnida. In: Social Insects, Vol. 4 (Hermann, H. R., ed.).
Academic Press, New York.736 K. S. Powers & L. Avilés
Byrom, A. E. & Krebs, C. J. 1999: Natal dispersal of juvenile arctic ground squirrels in the boreal
forest. Can. J. Zool. 77, 1048—1059.
Caraco, T., Uetz, G. W., Gillespie, R. & Giraldeau, L. 1995: Resource consumption variance within
and among individuals: on coloniality in spiders. Ecology 76, 196—205.
Cockburn, A., Scott, M. P. & Scotts, D. J. 1985: Inbreeding avoidance and male-biased dispersal in
Antechinus spp. (Marsupialia: Dasyuridae). Anim. Behav. 33, 908—915.
Dobson, F. S. 1982: Competition for mates and predominant juvenile male dispersal in mammals.
Anim. Behav. 30, 1183—1192.
Evans, T. A. 1998: Factors influencing the evolution of social behaviour in Australian crab spiders
(Araneae: Thomisidae). Biol. J. Linn. Soc. 63, 205—219.
Forero, M. G., Donazar, J. A. & Hiraldo, F. 2002: Causes and fitness consequences of natal dispersal
in a population of black kites. Ecology 83, 858—872.
Furey, F. E. 1998: Two cooperatively social populations of the theridiid spider Anelosimus studiosus in
a temperate region. Anim. Behav. 55, 727—735.
Gandon, S. 1999: Kin competition, the cost of inbreeding and the evolution of dispersal. J. Theor. Biol.
200, 345—364.
Greenwood, P. J. 1980: Mating systems, philopatry and dispersal in birds and mammals. Anim. Behav.
28, 1140—1162.
Gundermann, J. L., Horel, A. & Krafft, B. 1993: Experimental manipulations of social tendencies in
the subsocial spider Coelotes terrestris. Insect. Soc. 40, 219—229.
Hamilton, W. D. & May, R. M. 1977: Dispersal in stable habitats. Nature 269, 578—581.
Hawkins, B. A. & Lawton, J. H. 1995: Latitudinal gradients in butterfly body sizes: is there a general
pattern? Oecologia 102, 31—36.
Henschel, J. R. 1998: Predation on social and solitary individuals of the spider Stegodyphus dumicola
(Araneae, Eresidae). J. Arachnol. 26, 61—69.
Janzen, D. H. 1973: Sweep samples of tropical foliage insects: effects of seasons, vegetation types,
elevation, time of day, and insularity. Ecology 54, 687—708.
Johannesen, J. & Lubin, Y. 2001: Evidence for kin-structured group founding and limited juvenile
dispersal in the sub-social spider Stegodyphus lineatus (Araneae, Eresidae). J. Arachnol. 29,
413—422.
Johnson, C. N. 1986: Sex-biased philopatry and dispersal in mammals. Oecologia 69, 626—627.
Johnson, M. L. & Gaines, M. S. 1990: Evolution of dispersal: theoretical models and empirical tests
using birds and mammals. Annu. Rev. Ecol. Syst. 21, 449—480.
Jones, T. C. & Parker, P. G. 2000: Costs and benefits of foraging associated with delayed dispersal in
the spider Anelosimus studiosus (Araneae, Theridiidae). J. Arachnol. 28, 61—69.
Jones, T. C. & Parker, P. G. 2002: Delayed juvenile dispersal benefits both mother and offspring in the
cooperative spider Anelosimus studiosus (Araneae: Theridiidae). Behav. Ecol. 13, 142—148.
Kim, K. W. 2000: Dispersal behaviour in a subsocial spider: group conflict and the effect of food
availability. Behav. Ecol. Sociobiol. 48, 182—187.
Krafft, B. 1979: Organisations des societes d’araignees. J. Psychol. 1, 23—51.
Krafft, B., Horel, A. & Julita, J. M. 1986: Influence of food – supply on the duration of the gregarious
phase of a maternal – social spider, Coelotes terrestris (Araneae, Agelenidae). J. Arachnol. 14,
219—226.
Kullmann, E. 1972: Evolution of social behavior in spiders (Araneae: Eresidae and Theridiidae). Am.
Zool. 12, 419—426.
Levi, H. W. 1956: The spider genera Neottiura and Anelosimus in America (Araneae: Theridiidae).
T. Am. Microsc. Soc. 75, 407—421.
Levi, H. W. 1963: The American spiders of the genus Anelosimus (Araneae, Theridiidae).
T. Am. Microsc. Soc. 82, 30—48.
Lubin, Y., Hennicke, J. & Schneider, J. 1998: Settling decisions of dispersing Stegodyphus lineatus
(Eresidae) young. Isreal J. Zool. 44, 217—225.
MacArthur, R. H. 1972: Geographical Ecology. Harper & Row, San Francisco.
Moore, J. & Ali, R. 1984: Are dispersal and inbreeding avoidance related? Anim. Behav. 32,
94—112.
Motro, U. 1991: Avoiding inbreeding and sibling competition: the evolution of sexual dimorphism for
dispersal. Am. Nat. 137, 108—115.Natal Dispersal Patterns of a Subsocial Spider 737
Murray, B. G. 1967: Dispersal in vertebrates. Ecology 48, 975—978.
Negro, J. J., Hiraldo, F. & Donazar, J. A. 1997: Causes of natal dispersal in the lesser kestrel:
inbreeding avoidance or resource competition? J. Anim. Ecol. 66, 640—648.
Pasquet, A. & Krafft, B. 1992: Cooperation and prey capture efficiency in a social spider, Anelosimus
eximius (Araneae, Theridiidae). Ethology 90, 121—133.
Perrin, N. & Mazalov, V. 1999: Dispersal and inbreeding avoidance. Am. Nat. 154, 282—292.
Perrin, N. & Mazalov, V. 2000: Local competition, inbreeding, and the evolution of sex – biased
dispersal. Am. Nat. 155, 116—127.
Plateaux-Quénu, C., Horel, A. & Roland, C. 1997: A reflection on social evolution in two different
groups of arthropods: halictine bees (Hymenoptera) and spiders (Arachnida). Ethol. Ecol. Evol.
9, 183—196.
Riechert, S. E. 1985: Why do some spiders cooperate? Agelena consociata, a case study. Fla. Entomol.
68, 105—116.
Roeloffs, R. & Riechert, S. E. 1988: Dispersal and population—genetic structure of the cooperative
spider, Agelena consociata, in West African rainforest. Evolution 42, 173—183.
Ruttan, L. M. 1990: Experimental manipulations of dispersal in the subsocial spider, Theridion
pyramidale. Behav. Ecol. Sociobiol. 27, 169—173.
Rypstra, A. L. 1986: High prey abundance and a reduction in cannibalism: the first step to sociality in
spiders (Arachnida). J. Arachnol. 14, 193—200.
Rypstra, A. L. 1989: Foraging success of solitary and aggregated spiders: insights into flock formation.
Anim. Behav. 37, 274—281.
Schneider, J. M. 1995: Survival and growth in groups of a subsocial spider (Stegodyphus lineatus).
Insect. Soc. 42, 237—248.
Schoener, T. W. & Janzen, D. H. 1968: Notes on environmental determinants of tropical versus
temperate insect size patterns. Am. Nat. 102, 207—224.
Seibt, U.7 & Wickler, W. 1990: The protective function of the compact silk nest of the social
Stegodyphus spiders (Araneae, Eresidae). Oecologia 82, 317—321.
Tallamy, D. W. & Wood, T. K. 1986: Convergence patterns in subsocial insects. Annu. Rev. Entomol.
31, 369—390.
Tonkyn, D. W. & Plissner, J. 1991: Models of multiple dispersers from the nest: prediction and
inference. Ecology 72, 1721—1730.
Vollrath, F. 1986: Environment, reproduction and the sex ratio of the social spider Anelosimus eximius
(Araneae, Theridiidae). J. Arachnol. 14, 267—281.
Vollrath, F. 1987: Growth, foraging, and reproductive success. In: Ecophysiology of Spiders (Nentwig,
W., ed). Springer–Verlag, New York. pp. 357—370.
Ward, D. & Lubin, Y. 1993: Habitat selection and the life history of a desert spider, Stegodyphus
lineatus (Eresidae). J. Anim. Ecol. 62, 353—363.
Waser, P. M. 1985: Does competition drive dispersal? Ecology 66, 1170—1175.
Waser, P. M. & Jones, W. T. 1983: Natal philopatry among solitary mammals. Q. Rev. Biol.
58, 355—390.
Waser, P. M., Austad, S. N. & Keane, B. 1986: When should animals tolerate inbreeding? Am. Nat.
128, 529—537.
Wickler, W. & Seibt, U. 1993: Pedogenetic sociogenesis via the Ôsibling-routeÕ and some consequences
for Stegodyphus spiders. Ethology 95, 1—18.
Young, A. M. 1982: Population Biology of Tropical Insects. Plenum Press, New York.
Received: February 11, 2003
Initial acceptance: April 19, 2003
Final acceptance: May 27, 2003 (S. A. Foster)You can also read
