Behavioral Ecology Vol. 9 No. 4: 584-387
Spider-web kleptoparasites as a model for
studying producer-consumer interactions
linden E. Higgins* and Ruth E. Buskirkb
•Department of Zoology, University of Texas at Austin, Austin, TX 78712, USA, and Instituto de
Ecologia, Universidad National Autonoma de Mexico, Apdo. Post 70275, Mexico City, Mexico, and
••Division of Biological Sciences, University of Texas at Austin, Austin, TX 78712, USA
In this study, we documented that the kleptoparasitic spiders Argyrodes etevatus consume and assimilate web material from the
host spider Nephila elatripts. We also demonstrated quantitatively that the amount of web material consumed by the kleptoparasite is equivalent to the amount of insect material comsumed when host vigilance is low, as expected when foraging conditions
are very good. Argyrodes vary in their impact on their hosts, as they may steal large prey, small prey, or silk. This host-kleptoparasite interaction is therefore an ideal system for experimentally examining a variable producer—consumer interaction. We
compare our experimental results to published experiments showing that the impact of Argyrodes on a Nephila host can be
deleterious when foraging conditions are poor. Key words: Argyrodes, commensalism, kleptoparasitism, Nephila, parasitism.
[Behov Ecol 9:384-387 (1998)]
S
tudies of parasitic relationships traditionally emphasize
specialized traits and long-term adaptations. As Price
(1980) has pointed out, functional response strategies such as
food switching are often not possible for parasites. Yet many
interspecific interactions such as parasitism and commensalism are variable in nature. Existing classification systems do
not reflect the complex dynamics of interactions that are possible between two individual organisms when one is producing
and the other is consuming a renewable resource. In particular, whether an interaction is actually commensal (where neither organism profits at the disadvantage of the other) or
parasitic (where the producer or host suffers significant fitness
consequences due to the interaction) may depend greatly on
the current condition of the producer and the current feeding strategy of the consumer. Here, we report on one example
in which we have quantified how much the consumer it gaining from the producer in a situation where the consumer's
behavior is variable.
Many kinds of arthropods opportunistically take insects
from spiders' webs (reviewed in Vollrath, 1987). Several spiders in the genus Argyrodes (Araneae: Theridiidae) often specialize in this kleptoparasitic behavior, in fact, only a few species are reported to build their own webs (Canglialosi, 1997;
Eberhard, 1979; Exline and Levi, 1962). Previous reports suggested that some Argyrodes cut silk out of the host web (Cangialosi, 1991; Grostal and Walter, 1997; Rayor L, personal communication; VoUrath, 1987).
We have observed individual A. devatus removing web material from the orb webs of the host spider Nephila davipes
(Araneae, Tetragnathidae), cutting and collapsing sections up
to 4 cm in diameter. The kleptoparasite gathers the web material into its chelicerae and moves off the orb into a safe area
of the web. Orb webs contain physiologically important compounds (Tillinghast and Christenson, 1984; Tulinghast and
Townley, 1987; Townley et ad., 1991; Vourath et *L, 1991), and
spiders spinning viscid silk orbs often ingest their orbs at the
end of each foraging bout (PeahaQ, 1871; Townley and Tillinghast, 1988). Because these web components are valuable to
Addrcn correspondence to L. EL Higgins. E-mail; UndenOmaiL
utexas.edu.
Received 11 August 1997; accepted 8 January 1998.
O 1998 International Society for Behavioral Ecology
the host, consuming orb web material should also be nutritionally beneficial to the kleptoparasite. However, it was not
previously known if the silk gathered by the kleptoparasites
was consumed. The removal of pieces of orb web by the kleptoparasites can have two negative effects on the host: it prevents the host from recycling its own orb web, and it creates
holes, reducing the effectiveness of the orb web as a trap
(Grostal and Walter, 1997).
The goal of the current study was to determine experimentally whether the silk collected by A. elevatus was consumed,
and whether this silk formed a significant portion of the diet
of these spiders. We expect the importance of silk in the diet
to vary with host prey capture, but the significance of the
behavior to the host will depend in part on whether the kleptoparasites are present under conditions of low prey capture
by the host Therefore, we looked for patterns of variation in
kleptoparasite load per female among natural populations differing in average prey-capture success. We emphasize that although there are many anecdotes concerning producer-consumer interactions where a biological secretion is being consumed, there are few systems that present the opportunity for
manipulation such as the Nephilo-Argyrodes interaction.
Kleptoparasite abundance on host orb-webs
Methods
We observed populations of N. davipes in six different habitats in Mexico between 1988 and 1990 and systematically
counted the number of all Argyrodes present on the orb web
and barrier structures during regular, bimestrial censuses of
sexually mature females (Table 1). At each census,we marked
all adult host females with Testers paint In cases when we
observed a host more than once, one randomly selected observation was included in this analysis. Nephila davipes in
some habitats tend to build interconnected webs, and aggregations may have higher kleptoparasite loads (Elgar, 1989).
Therefore, we considered only webs built by solitary females.
Results
In some populations, adult female N. davipes routinely had
kleptoparasites in their webs (Figure 1). There was little variation in kleptoparasite density per web between years of study
in the six sites (Mann-Whitney U tests, all p 2 .02). When
Higgins and Buskirk • Spider-web kleptoparasites
385
Table 1
Prey capture at six sites in
Site
Coordinate*
Playa
Escondida 18°S0' N, 95° W
Nanciyaga
18°30' N, 95* W
Fortln
de las Flores 19° N, 97° W
Tehuacan
18°20' N, 97°30' W
Arroyo Frio —
ChameU
19°3O' N, 105° W
Altitude,
m
5
100
1000
1500
1000
50
Seasonality
Average
prey
capture
rate
Cold
Cold
1.2
3.1
Cold
Cold, dry
Cold, dry
Dry
3.8
3.0
—
2.2
* Number of prey captured per female per 12 diurnal h, averaged
over 2 years of observation (Higgins LE, personal observation).
different years were pooled, the median number of kleptoparasites per host varied significantly among the six populations studied (Kruskal-Wallis = 185.2, df = 5, p < .001), with
much lower abundances at the higher altitude, drier sites of
Tehuadn and Arroyo Frio (Figure 1). At all the other sites,
most adult female hosts had kleptoparasites in their webs, and
5-20% of the N. davipts females had more than 10. Our data
show no correlation between a population's average prey-capture rates (Table 1) and its kleptoparasite abundance.
Kleptoparasite consumption of web material
Methods
We collected Argyrodes devatus from N. davipawebs in Brazos
Bend State Park, Fort Bend County, Texas, USA, and housed
them on N. davipes webs in a greenhouse. To test whether
the web material gathered is actually consumed, we kept
groups of five randomly chosen A. devatus females for 2 days
on either nonradioactive, unoccupied webs with eight dead
(killed by freezing), radioactive Drosophila mdanogaster or radioactive, unoccupied webs with eight dead, nonradioactive
flies. (A comparison of radioactive and nonradioactive flies
verified that there was no difference in fly dry weight between
treatments; ANOVA; F{1S9) •» 0.005, p = .942; mean weight
(radioactive) = 0.207 mg, SE = 0.013; mean weight (nonradioactive) = 0.209, SE = 0.020). In both treatments, we
checked the webs after 24 h, counted the remaining flies, and
restored the number available to eight. After 48 h, we collected and killed by freezing all kleptoparasites and collected
the radioactive orbs. The kleptoparasites were homogenized
in 400 uj distilled, deionized water, from which 100-uJ samples
were tested for radioactivity.
Radioactively labeled webs were obtained from four N. davipes females (from the same locality) that had been fed 10
ui of '*C-U-glucose (5 \i£i). The host spiders were allowed to
spin and recycle at least one orb web to assure that die label
was incorporated into both protein and viscid components of
the orb. We removed the spiders from the webs immediately
before introducing the kleptoparasites. Each host spider spun
2-4 orbs used in the experiment; a total of 12 webs were used.
We obtained four batches of radioactive flies by feeding them
red wine to which 14C-U-giucose had been added (5 u.Ci in
200 uj). To determine radioactivity per unit dry weight, we
dried 31 flies and all radioactive orb webs for at least 7 days
over calcium sulfate. Mass and radioactivity were determined
for individual flies from r**r\\ batch and for samples of each
radioactive orb. We dien used the radioactivity per unit dry
weight for each food source to convert die radioactivity of die
1
2
3
4
5
S10
S20
kleptoparasites per female
Figure 1
Frequency of kleptoparasites on webs of adult female Ntphila
davipts, by year, in six different rites in Mexico. Nan, Nanciyaga;
PE, Playa Escondida; FF, Fordn de las Flores; Teh, Tehuacan; AF,
Arroyo Frio; Ch, Chamrla.
kleptoparasites to micrograms-dry weight consumed (in the
case of radioactive flies, we used die mean radioactivity for
die batch used to feed each group of kleptoparasites). For
flies, die radioactivity (mean cpm per mg dry weight per
batch) ranged from 48,493 (SE = 24,973) to 100,689 (SE =
27,479). For ort>web material, the radioactivity (cpm per mg
dry weight for 12 webs) ranged from 840 to 18,089.
Results
In both treatments, individual A. devatus females were observed eating both flies and silk. By converting die radioactivity of die kleptoparasites to milligrams consumed of flies or
web material, we determined that significant amounts of web
material were eaten by die kleptoparasitic spiders. In fact,
there was no difference between treatments in die amount of
radioactively labeled food consumed (Figure 2, n = 39 fed
radioactive flies, n «• 36 fed radioactive webs; KolmogorovSmirnov D = 0.244, p = .2). There was also no difference
Behavioral Ecology Vol. 9 No. 4
388
20
• radioactive flies
0 radioactive silk
15 -
10 -
5Flgure 2
Dry weight of material (micrograms) consumed by kleptoparasitic A. tUvatus females
when placed on radioactivety
labeled host webs with nonlabcled fruit flies (open bars) or
on nonlabeled host webs with
radioactively labeled fruit flies
(hatched bars).
f
0
2
between treatments in number of flies consumed (Kolmogorov-Smirnov D = 0.S5S, p = .423; mean = 10.25, SE = 0.83).
Although some individuals were highly radioactive in each
treatment, more than 15% of the individuals remained nonradioactive in both treatments. This verifies that radioactivity
in each A. tlevatus reflects consumption of radioactive food
rather than contamination through contact with radioactive
substrates.
There was variation among individual spiders in which type
of food was used. Large amounts of silk may be consumed: in
a trial run involving the same host species and both A. elevatus
and A. gtobosus, one individual consumed 800 fig dry weight
of web material in 24 h, about 40% of a female kleptoparasite's weight.
DISCUSSION
When Argyrodts devatus are presented widi both insect prey
and host web material as potential food sources, in the absence of host defense of either web or prey, they consume
both equally. Web material appears to be a significant nutritional source for these kleptoparasites, which would otherwise
be restricted to stealing small insects ignored by their hosts
with only occasional success in removing large prey items from
the hub (VoUrath, 1979, 1987). Insect prey in the host webs
represent a patchy resource for the kleptoparasite as well as
for the host. Therefore, parasitic spiders that can steal and
consume silk during periods of low prey-capture success by
their hosts would have an advantage over parasites that consume only insects and must either wait for die host to capture
prey or locate a new host web.
What is the origin of such behavior? Although viscid orbweaving spiders routinely tear down their webs (Carico, 1986)
and consume their own silk (Peakall, 1971; Townley and Tilnnghast, 1988), web-building spiders in the kleptoparasitic
family Theridiidae are not known to consume dieir webs (J.
Codffington, personal communication). Therefore, consumption of host silk by a kleptoparasite is not an elaboration of
existing web consumption behavior. In Argyrodes, silk consumption may be the modification of a different preexisting
behavior, namely, the theft of prey by cutting insects out of a
web, to a new behavior, the theft of silk by cutting web lines
containing no prey.
I
I I
I
I I I I
I I
I I I
I I
8 10 12 14 16 18 20 22 24 26 28 30 32
10 jig consumed
Kleptoparasite abundance can be high and may have a significant effect on host fitness (present study; Cangialosi, 1997;
Grostal and Walters, 1997). The effect on host fitness will vary
with kleptoparasite behavior Argpvdes have been reported on
various occasions to take insects ignored by the host, feed with
the host, steal prey captured by the host, and even displace
the host from its web and prey upon the host (Cangialosi
1997; Exline and Levi, 1962; Larcher and Wise, 1985; Robinson and Olazarri, 1971; Robinson and Robinson, 1973; Smith
Trail, 1980; Tanaka, 1984; VoUrath, 1979; Wise, 1982).
When Argpvda engage in purely kleptoparasitic behavior
(sharing a web and stealing prey and silk), the impact of the
kleptoparasite on the host and the host response to kleptoparasite activity probably depend largely on prey abundance. However, we have found that kleptoparasite load per host is not simply a function of site-specific prey capture rates (Table 1, Figure
1). In general, in times or areas of high prey capture rates, the
host exhibits less territorial defense of the web, tolerating interand intraspecific neighbors in aggregations (Rypsea, 1981,1988,
1989; Uetz 1988) and also tends to ignore smaller prey (Higgins
and Buskirk, 1992). In contrast, during periods or in areas of
low prey capture rates, Ncphila spiders take prey of a greater size
range (Higgins and Buskirk, 1992) and defend their prey more
aggressively against kleptoparasites (\foflrath, 1987). Therefore,
one could predict that incidence of theft of insects in the orb
by A. devatus would be determined mainly by die food supply,
and thus the tolerance, of the host
The nature of this two-species interaction should vary predictably with food resources. As host foraging success declines, we
expect the consumer's effect on the host to become more detrimental and more parasitic In the current study, we Mmnlafrd
conditions of high prey abundance by removing the host spider
and providing both insect prey and web material as food. Under
these conditions, die kleptoparasites feed equally on both food
sources, and we expect their effect on die host spider to become
negligible and the interaction to more closely resemble commrmatnm Results fam Ctoatal and Walters (1997) provide evidence for the parasitic nature of the interaction at low preycapture levels. In their experiment providing N. ptunapa juvenile frmaV* with medium amounts of food, they found a significant detrimental effect of A. antipodiamis kleptoparasites that
could not be explained by either sQk removal or lowered prey
capture rates alone.
Higgins and Buskirk • Spider-web kleptoparasite*
There are many anecdotes but no other quantitative records
of an animal consuming and assimilating the biological secretions synthesized by another species. Indeed, the detritus component of food webs, which includes animal secretions, has not
been well described quantitatively (PoHs, 1995). Many invertebrates secrete mucous traps for fitter-feeding on plankton and
paniculate matter. Animals such as tube-worms, corals, and oysters are known to have commensals thai feed on *rrti* or leftover food particles in the vicinity of the mucous trap. In theory,
these commensals might consume the mucous as well as food.
The commensal relationship of the pea crabs Pinnotheres spp.
living with oysters and tube worms his been observed in detail
(Rohde 1982), but no mucous feeding has been observed. The
most analogous situation to web consumption by kleptoparasitic
spiders is found among anfmah associated with corals. A number
of shrimp, crabs, and goby fish are known to consume the detritus-laden mucous secreted by corals (Patton, 1974). Under experimental conditions, goby fish (Pamgobiodon) ate both mucus
and coral tissue (Patton, 1974).
Interactions that grade between purely commensal and dearly
parasitic include a number of cases of fish that consume secretions or regenerating body parts of other fish species. Some fish,
such as mucus-feeding catfish, scale-feeding Characidar and Pimelodidae, fin-eating piranhas, and tail-eating electric fishes specialize on such feeding, perhaps extensively harming the producer (Lundberg et aL, 1996; Winemffler 1990). These hostconsumer interactions are inferred from stomach content analyses during community ecology studies. The behaviors are largely
unstudied (however, see Winemiller 1990), and consequences to
die host are unknown. As Rohde (1982) has pointed out, commensatism and mutualism are closely related to parasitism. The
boundary between these phenomena and parasitism is often indistinguishable because of insufficient knowledge or because die
interaction is variable.
Experimental manipulations have demonstrated that Argywdes
behavior varies from theft of prey to theft of silk, and that Argjroda activity can have a detrimental effect on the producer
(see also Grostal and Walter 1997). The variability of berth host
and kleptoparasite behavior and our ability to manipulate and
measure the effects of die relationship through controlled experiments in die laboratory make this a useful system for better
understanding producer-consumer interactions.
The population studies in Mexico were supported by grants to LH. from
the Organization of American Slates and from the National Autonomous
University of Mexico (UNAM). The Institute de Ecologia, UNAM, provided logistical support. The laboratory portion of this research was supported by a grant from the National Science Foundation (TfiN-922094).
The Division of Biological Sciences of the University of Texas at Austin
provided greenhouse space, and collecting permits were granted by Texas
Parks and Wildlife. In Mexico, several people generously allowed LH. to
work on their piupeity. L. Forbes and S. Ayala (Forttn), C Rodriguez
(Nanciyaga), F. Aguflar (Arroyo Frio), and the management of Hotel
Playa Escondida. Permission to work at Oiamcla was granted by the Institute de Bkrfogfa, UNAM, and permission to work at Tehuacan cactus
garden was granted by the Institute National de Ecologfa. We thank M.
A. Rankin for use of laboratory facilities.
REFERENCES
Cangialosi KR, 1991. Attack strategies of a spider kleptoparasite: effects
of prey availability and host colony size. Anim Behav 41:699-648.
rangjaWvd KR, 1997. Foraging venuiKty and die influence of host availability oa Argjmdo trigonum (Araneae, Theridiidae). J Anchnol 25:
182-193.
Carico JE, 1986. Web removal patterns in orbweaving spiders. In: Spiders:
webs, behavior and evolution (Shear WA, ed). Stanford, California:
Stanford University Press; 306-318.
587
Eberhard WG, 1979. Argymde *M-*II*UI (Theridiidae): a web that is not
a snare. Psyche 86:407-413.
Elgar MA, 1989. Kkptoparastism: a cost of aggregating for an orb-weaving spider. Anim Behav 37:1052-1055.
Fjdine H, Levi HW, 1962. American spiders of the genus Argjrodc (Araneae, Theridiidae) Bull Mus Comp Zool Harvard 127:75-204.
Grostal P, Walter DE, 1997. Kleptoparasites or commensals? Effects of
Argywdc andpoeHaaa (Araneae: Theridiidae) on Ntp/aia pbanpa
(Araneae: Tetragnadudae). Oecologia 111570-674.
Higgins LE, Buskirk RE, 1992. A trap-building predator exhibits different
tactics for different aspects of foraging behaviour. Anim Behav 44.-485499.
Larcher SF, Wise D, 1985. Experimental studies of the interactions between a web-invading ipider and two host species. J Arachnol 13:4359
Lundberg JG, Fernando CC, Albert JS, Garcia M, 1996. Magostrmarchus,
a new genus with two new species of electric fishes (Gymnoafbrmes:
Apteronoadae) from the Amazon River Basin, South America. Copeia
1996 (3)^57-670.
Patton WK, 1974. Community structure among die animal* inhabiting
die coral PodUopma damiaxrms at Heron Island, Australia. In: Symbiosis
in die sea (Vernberg WB, ed). Columbia: University of South Carolina
Press; 219-243.
Peakall DB, 1971. Conservation of web proteins in the spider Arantus
dtadtmatus-J Exp Zool 176257-264.
Polis GA, 1995. Complex food webs. In: Complex ecology (Patten BC,
Jorgensen SE, eds). Englewood Qifis, New Jersey: Prentice-Hall; 513548.
Price PW, 1980. Evolutionary biology of parasites. Princeton, New Jersey.
Princeton University Press.
Robinson MH, OlazarriJ, 1971. Units of behavior and complex sequences
in die predatory behavior of Argiope argtntata (Fabricius): (Araneae:
Araneidae) Smithjon Contrib Zool 66:1-36.
Robinson MH, Robinson BC, 1973. Ecology and behavior of the giant
wood ipider Ncpfala ~""'t)» (Fabricius) in New Guinea. Smithson
Contrib Zool 149:1-76.
Rohde K, 1982. Ecology of marine parasites. New Tfbrk: University of
Queensland Press.
Rypstra AL, 1981. The effect of kleptoparasitism on prey consumption
and web relocation in a Peruvian population of the spider Nephiia
damps. Oikos 37:179-182.
Rypstra AL, 1983. The importance of food and space in limiting webspider densities; a test using field enclosures. Oecologia 59312-316.
Rypstra AL, 1989. Foraging success of solitary and aggregated spiders:
insights into flock formation. Anim. Behav. 37274-281.
Smith Trail DRR, 1980. Predation by Argywda on solitary and communal
spiders. Psyche 87349-355.
Tanaka K, 1984. Rate of predation by a kleptoparasitic ipider, Argymdo
fissifnms, upon a large host spider, Ageltna timbata.] Arachnol 12363367.
Tillinghast EK, Christenson T, 1984. Observations on die chemical composition of the web of Nephiia davipts (Araneae, Araneidae) J Arachnol
12^9-74.
^
Tillinghatt EK, Townley M, 1987. Chemistryrphysical properties, and synthesis of Araneidae orb webs. In: Ecophysiology of spiders (Nentwig
W, ed). New 'fork: Springer Verbg; 203-210.
Townley M, Berstein DT, Gallagher KS, TiDinghast EK, 1991. Comparative
study of orb web hygiuacupicity and adhesive spiral composition in
three Araneid spidersj Exp Zool 259:154-165.
Townley M, Tuunghast EK, 1988. Orb web recycling in Arantui ctwaticus
(Araneae, Araneidae) with an cmphaiHS on die adhesive spiral component, Gahamidf.J Arachnol 16303-319.
Uetz G, 1988. Group foraging in colonial web-building qxders: evidence
for riifc«njinvity. Behav Ecol Scoobiol 22265-270.
vbOnuh F, 1979. Behaviour of die kleptoparasitic ipider Argyroda dtvatus.
Anim Behav 27515-521.
VoDrath F, 1987. Kleptobians in spiders. In: Ecophysiology of spiders
(Nentwig W, ed). New % * Springer Verlag; 274-286.
VbOradi F, Fairbrother WJ, Wfflianu RJP, TiBinghast EK, Berstein DT, Gallagher KS, Townley M, 1991. Compounds in die droplets of die orb
spider's viscid spiral. Nature 345526-528.
WmemSler KO, 1990. Spatial and temporal variation in tropical fish trophic networks. Ecol Monogr 60331-367.
Wise DH, 1982. Predation by a commensal spider, Argyrodts trigonum,
upon its hose an experimental study. J Arachnol 10:111—116.