Table Of Content2002. The Journal of Arachnology 30:31-38
TWO
POPULATION DYNAMICS OF SPECIES OF
KLEPTOPARASITIC SPIDERS UNDER DIFEERENT
HOST AVAILABILITIES
Tadashi Miyashita: Laboratory of Biodiversity Science, School of Agriculture and
Life Sciences, University of Tokyo, Tokyo 113-8656 Japan.
Email: [email protected]“tokyo.ac.jp
ABSTRACT. Kleptoparasitic spiders are known to have a close association with host spiders, yet there
have been few studies demonstrating how host availability influences the dynamics of kleptoparasites.
Field surveys were conducted at five sites differing in host composition in sub-tropical areas in Japan, at
about two-months intervals. Argyrodes flavescens and A. bonadea were both found more frequently on
webs of two Nephila species than expected from the web areas they occupied among webs of all web
spiders. Seasonal dynamics of Argyrodes changed greatly according to whether N. clavata was present or
not, indicating the importance of Nephila on Argyrodes populations. The peak density ofA. bonadea came
earlier than that of A. flavescens. Because A. flavescens is known to limit the number of A. bonadea on
host webs, the decrease in the density ofA. bonadea may be due to the effect of interspecific competition
by A. flavescens.
Keywords: Interspecific competition, parasite, Theridiidae, phenology
Spiders in the genus Argyrodes Simon 1864 A. flavescens O. Pickard-Cambridge 1880 and
are often called kleptoparasites that rely al- A. bonadea (Karsch 1881), are commonly
most exclusively on host spiders. However, found on orb-webs of various spider species.
the interaction between Argyrodes and their Preliminary observations revealed that a large
hosts is complex: Argyrodes can be klepto- number of the two species was found on the
parasites, commensals, or predators to their webs of Nephila clavata and N. niaculata (Fa-
hosts depending on the species and host con- bricius 1793). These two Nephila species have
ditions (e.g., Trail 1980; Tanaka 1984; Larcher different phenologies, the former emerging
&
Wise 1985; Whitehouse 1986; Cangialosi later in the season. Also, the distributions of
1997). These close associations lead to the in- the two species differ, N. maculata lives all
ference that population dynamics of Argyro- over the island while N. clavata inhabits only
des is highly dependent on host availability. the northern part of the island. These charac-
Vollrath (1987) demonstrated the dynamics of teristics enable us to estimate the importance
two Argyrodes species and their host Nephila of host availability.
clavipes (Linnaeus 1767). However, there In this paper I examined seasonal dynamics
have been no studies showing how changes in of the two Argyrodes species and their poten-
host species composition influences Argyro- tial host spiders in five sites differing in host
des dynamics. Ideally such a causal relation- species compositions. I hypothesize that 1) the
ship should be evaluated by field experiments Nephila species are the preferred host for Ar-
in which a particular host is removed, but pop- gyrodes, and 2) the presence or absence of
ulation manipulation on a large scale suffi- Nephila clavata changes population dynamics
cient to change host availability is impractical. of Argyrodes greatly.
Examining the variation of kleptoparasite dy-
METHODS
namics in areas differing in host availability
seems to be the only way to estimate the Field studies were conducted at four sites
strength of associations between the host and on Okinawa Island, Nakagusuku (NK), Nan-
kleptoparasite at the population level. gusuku (NG), Shoshi (SH), Nakijingusuku
On Okinawa Island located in the south- (NJ), and at one site on Iheya Island (IH),
western part of Japan, two Argyrodes species, southwestern Japan. The climate of these sites
31
—
THE JOURNAL OF ARACHNOLOGY
32
is sub-tropical, with an average temperature of and Nj is the total number of Argyrodes sp.
j
22.6 °C and an annual rainfall of 2,100 mm. on host species j. Hosts harboring at least ten
Previous observations revealed that Nephila Argyrodes or those occupying more than 30%
clavata, a major host for Argyrodes, lives at of the total web areas of all species combined
NK
all sites except for which is located at the were used for the analysis. Significance level
southern part of Okinawa Island, Iheya Island was adjusted by the sequential Bonferroni
lies about 60 km away from Okinawa Island method (Sokal and Rohlf 1995) for each sea-
and is much smaller (about 20 km^) than that son.
of Okinawa Island (about 1,199 km^). Thus I
RESULTS
expected densities and/or species richness of
host spiders to be low on that island. Dynamics of Argyrodes and their host.
m
I established two 50 lines along the road- The kleptoparasitic spiders found in this sur-
side in forests at each site, and surveyed these vey were mostly A. flavescens and A. bona-
transects five times (four times for IH) from dea. Figure 1 shows seasonal changes in the
July 1997 to April 1998 at intervals of ap- density of the two Argyrodes spp. and web
NK
proximately 2-3 mo. I recorded all web spi- areas of host spiders in five study sites. In
mm
ders with body lengths larger than 4 liv- where N. clavata is absent, the dynamics of
m m
ing within 2 from the transect and 2 from web area were mostly determined by N. ma-
the ground. I recorded the spider body length, culata. Although the peak density of A. fla-
the vertical and horizontal web diameters, any vescens was delayed relative to that of host
prey being consumed, and any small insects web area, its density decreased abruptly in
remaining in the web. At the same time I November when N. maculata disappeared. In
counted and recorded the body length of all NG, SH and NK, however, N. clavata is abun-
Argyrodes found on the spider webs with cal- dant in November, and Argyrodes maintained
ipers. Because it was difficult to know the high densities in November. It is noteworthy
stage of Argyrodes in the field, I used body that the timing of peak density of the two Ar-
length as an indicator for the stage and deter- gyrodes species differed, with A. bonadea
mm
mined the smallest size of adults, viz., 3 reaching the peak earlier. Another important
mm
for A. flavescens and 2.5 for A. bonadea. point is that both Argyrodes densities declined
In this study, web areas of hosts instead of to low levels in January and April when web
density of host individuals was used for rep- areas of spiders other than Nephila remained
resenting host availability because the body at levels similar to those in November. The
size of host spiders varies greatly depending main species in this period were Leucauge
on the species and seasons. For instance, the blanda (L. Koch 1878), Cyclosa confusa Bos-
web of Nephila maculata is much larger than enberg & Strand 1906 and Neoscona scylla
that of most other spiders, so that the amount (Karsch 1879). In IH where N. clavata was
of habitat and food resources available to Ar- not found on the census route, the density of
gyrodes may vary greatly. Argyrodes showed a peak in August and then
The density of each Argyrodes on a partic- dropped sharply in November, which is simi-
ular host species (no./cm^) was calculated as lar to the situation in NK. Unlike other study
follows, S N,/S Aj, where N, is the number of sites, the density of A. bonadea was much
Argyrodes on the web of a particular host higher than that of A. flavescens.
i'*^
species and Aj is the web area of the web. Percentage of adult Argyrodes.—The per-
Data from the two transects were combined at centage of adult individuals was calculated
A
each site. binomial test was performed to separately for areas where both Nephila spe-
ascertain whether each Argyrodes prefers a cies were present (NG, SH, NJ) and Nephila
particular host spider species. The null hy- clavata was absent (NK, IH). In areas where
pothesis was that the total number of Argy- both Nephila species were present, seasonal
rodes on webs of host species (Nj) is deter- change in the percentage of adults differed
j
mined by the proportion of the web area of greatly between the two Argyrodes (Fig. 2).
that host, i.e., The peak occurrence of adult A. flavescens
= Ays S was found in autumn while that ofA. bonadea
N, A, Nj,
• was in spring and early summer. In areas
where Aj is the total web area of host species where Nephila clavata was absent, the differ-
MIYASHITA—DYNAMICS OF KLEPTOPARASITIC SPIDERS 33
in
sites
5
in
spiders
web
other
and
species
Nephila
two
the
of
areas
web
and
species,
Argyrodes
two
the
of
numbers
the
of
dynamics
Seasonal
—
1.
Figure
Okinawa.
S9poj^8jY JO ’o^
THE JOURNAL OF ARACHNOLOGY
34
BothNephila present Nephila clavata absent
Month
—
Figure 2. Percentage of adult Argyrodes in areas ;vith and without Nephila clavata. Numerals in the
figure represent sample size.
ence was less conspicuous due to the high per- in November were small plant hoppers in all
centage of adult A. flavescens in spring. Ar- study sites.
gyrodes bonadea showed a similar seasonal
DISCUSSION
pattern in the two types of areas.
—
A
Host preference ofArgyrodes. total of The dynamics of the two Argyrodes species
18 species of web spiders was recorded in- were largely affected by the phenologies of
cluding all sites and seasons (Table 1). Twelve Nephila species. This is clearly illustrated by
species were found to be hosts for A. flaves- the following findings: 1) where there is no
cens, and 14 were hosts for A. bonadea. N. clavata (NK and IH), densities of Argyro-
The results of the binomial tests (Table 2) des declined rapidly in November when N.
revealed that A. flavescens had a strong ten- maculata had disappeared; but where both Ne-
dency to prefer Nephila clavata in August and phila species were present, the density in-
November, although no preference was found creased in November for A. flavescens and de-
in July when Nephila clavata was still small creased slightly for A. bonadea’, 2) preference
in body size. Nephila maculata was preferred for Nephila webs was prominent, especially
in July probably because Nephila was already by A. flavescens. The first finding is particu-
large. Besides the two Nephila species, only larly good evidence for the importance of Ne-
Argiope minuta was preferred significantly. phila on Argyrodes dynamics because this can
Leucauge blanda^ and Cyclosa confusa had be viewed as a “natural experiment” in which
significantly fewer A. flavescens on their webs one major host was “removed”. Grostal &
than expected from their web areas. Walter (1999) revealed a similar result show-
Argyrodes bonadea also preferred N. cla- ing that Nephila spp. were the preferred hosts
vata in August and November, but the pref- for A. antipodianus. The reason why Nephila
erence for N. maculata was obscure. Unlike webs are suitable for Argyrodes may be that
A. flavescens, Cyrtophora moluccensis, which these webs have a barrier web on both sides
builds large, horizontal and tightly-meshed of the capture web, providing a space for liv-
webs, was a preferred host for A. bonadea. ing. The significance of barrier webbing for
Leucauge blanda had fewer A. bonadea than Argyrodes has already been argued by several
&
expected from its web area. — researchers (Whitehouse 1986 1997; Can-
Prey density on host webs. Figure 3 gialosi 1997). Comparing the two Nephila
shows seasonal changes in prey density on species, N. clavata has a more elaborate bar-
Nephila webs. In all areas, prey density on rier web and N. maculata sometimes lacks a
host webs increased in November and then de- barrier web (unpub. obs.). This may explain
creased markedly in January. The main prey why N. clavata was preferred more frequently
>
A—
MIYASHIT DYNAMICS OF KLEPTOPARASITIC SPIDERS 35
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36 THE JOURNAL OF ARACHNOLOGY
—
Table 2. Results of binomial test to assess whether each Argyrodes species prefers a particular host
spider. The null hypothesis is that an Argyrodes chooses a host spider in proportion to its web area.
Positive signs mean preference (+ ++ = p < 0.001, ++ = p < 0.01, + = p < 0.05), negative signs
mean avoidance ( = P < 0.001, = P < 0.01, — = p < 0.05).
Abbreviations for species name are the same as in Table 1.
Argyrodesflavescens
Host species
Site Month Nm Nc Av Cm Lb Ns Cc Am
NK Aug +++ — ns —
NG
.Jul ns ns ns
Aug ++ +
Nov ++ ns ns
SH Jul ++ + ns —ns ns
Aug ns + + + ns
Nov ns + + + + +
NJ Jul
Aug ns ns +
Nov ++ —
-h
IH Aug
Argyrodes bonadea
Host species
Site Month Nm Nc Av Cm Lb Ns Cc Am
NK Aug ++ —
ns
NG —
Jul ns ns ns
Aug ns +++ ns
Nov — + ns ns
SH
Jul ns ns ns
—
Aug + + A
Nov ns ns ns ns ns
NJ Jul ns ns -h
Aug ++ + + ns
Nov + ns
IH Aug ns ns
than N. maculata by the two Argyrodes, Other that of A. flavescens. This difference may be
studies have shown that Argyrodes spiders oL due to interspecific competition between the
ten live in Nephila webs (e.g., Elgar 1993) but two Argyrodes species. Miyashita (2001)
only a few of them have demonstrated the sea- demonstrated that experimental removal of A.
sonal dynamics of Nephila-Argyrodes sys= flavescens increased number of A. bonadea
terns. Vollrath (1987) showed that the dynam- within only 2 d, and the number of individuals
ics of A. elevatus and A, caudatus were removed was positively correlated with the
closely related to the number of N. clavipes in rate of increase in A. bonadea. Although this
Panama, yet no evidence was provided show- experiment indicated interspecific competition
ing that alternative host spiders were not re- on a small spatial scale, this effect is likely to
sponsible for this pattern. The present study extend up to regional scales. There is addi-
clearly demonstrates the importance of Ne- tional circumstantial evidence supporting the
phila as hosts for Argyrodes both from the likelihood of interspecific competition. In a
“natural experiment” and preference analysis. temperate area where only A. bonadea was
Another interesting point in the population present, Yasuda (pers. comm.) found that this
dynamics of the two Argyrodes is that the species is most abundant in mid-October
peak density of A. bonadea was earlier than which is the late adult period of N. clavata
A—
MIYASHIT DYNAMICS OF KLEPTOPARASITIC SPIDERS 37
by consuming prey abundant on host webs but
adjusts its life cycle by retarding its develop-
ment. It appears that A, flavescens has a more
opportunistic life cycle strategy than A. bon-
adea.
From winter to spring when the main hosts
were absent, Argyrodes spiders were found to
live on the webs of smaller orb-weavers such
as Leucauge blanda, Cyclosa confusa and
Gasteracantha mammosa, which were not
preferred in the presence of Nephila. White-
house (1988) found that the host range of A.
— antipodiana in winter was larger than that in
Figure 3. Seasonal change in prey density (no./
growing and reproductive seasons, probably
web area) on host spider webs. The 3 sites shown
here have both of the two Nephila species. because overwintering individuals need webs
for shelter only. However, the situation of Ar-
gyrodes in the present study is quite different
because I often observed Argyrodes ingesting
and 2 mo behind the peak of the web area. silk of host webs as well as stealing prey (un-
On Okinawa, however, A. bonadea showed a pub. obs.). The difference is mainly due to
peak in late August and the density decreased climate conditions: the present study was
in November, the beginning of the adult pe- made in the sub-tropics whereas the study by
riod in Okinawa. This means that A. bonadea Whitehouse was in a temperate region. Al-
living in regions without A. flavescens showed though it seems unlikely that sub-tropical Ar-
host-parasite dynamics similar to A. flaves- gyrodes can obtain sufficient food in winter,
cens. Accordingly, interspecific competition they may be able to survive the harsh period
by A. flavescens may have shifted the dynam- by living on unfavorable hosts. Grostal &
ics of A. bonadea to earlier seasons. An alter- Walter (1999) found no A. antipodianus on
native explanation is that the life cycle of A. webs of Leucauge sp. and Gasteracantha sp.
bonadea in sub-tropical Okinawa is different in Australia but the season they studied was
from that of the temperate area, which is un- the period when the main host Nephila was
related to competitive interactions with A. fla- present. It seems necessary to clarify the role
vescens. It would be difficult to test whether of non-preferred host for the maintenance of
there is a causal relationship between the dy- Argyrodes populations.
namics of the two Argyrodes species because
ACKNOWLEDGEMENTS
large scale experimental manipulation is nec-
essary. I thank Mary Whitehouse for comments on
Host composition appears to have a minor the manuscript, and Akira Shinkai, Takafumi
impact on the age structure of Argyrodes, es- Chida, Aya Shimazaki, Yasunori Maezono
pecially for A. bonadea (Fig. 2). The increase and Claire Cartan for assistance in the field.
in the proportion of adults in spring in areas This research was supported by Eujiwara Nat-
without N. clavata might have been an artifact ural History Foundation.
due to the small sample size (N = 8). Adults
LITERATURE CITED
of A. flavescens were found throughout the
year but the peak was in autumn when prey Cangialosi, K.R. 1997. Foraging versatility and the
on host webs were most abundant. If the in- influence of host availability in Argyrodes tri-
crease in prey availability had already been gonum (Araneae, Theridiidae). Journal of Arach-
nology 25:182-193.
initiated in October, this can explain the high-
Elgar, M.A. 1993. Inter-specific associations involv-
er proportion of adults in November, because
ing spiders: Kleptoparasitism, mimicry and mu-
spiderlings ofA. flavescens can reach maturity
tualism. Memoirs of the Queensland Museum
and produce egg sacs in a month (unpub.
33:411-430.
obs.). Contrarily, adults of A. bonadea were Grostal, P. & D.E. Walter. 1999. Host specificity
rarely found in autumn, suggesting A. bona- and distribution of the kleptoparasitic spider Ar-
dea does not accerelate its developmental rate gyrodes antipodianus (Araneae, Theridiidae) on
THE JOURNAL OF ARACHNOLOGY
38
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&
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