Social Encounters Between Male Brown Spiders, Loxosceles gaucho (Araneae, Sicariidae)

2007·7 MB·English

by  André Augusto Stropa

2007 (2008). The Journal ofArachnology 35:493^98
SOCIAL ENCOUNTERS BETWEEN MALE BROWN SPIDERS,
LOXOSCELES GAUCHO (ARANEAE, SICARIIDAE)
Andre Augusto Stropa: Rua Sargo, 84, Vinhedo, SP, CEP:13280-000, Brazil. E-mail:
astropa@gmaiLcom
ABSTRACT. Twenty-two interactions between males ofLoxoscelesgaucho Gertsch 1967 were investigated
in order to study its intrasexual interactions and level ofaggressiveness. Aggression by lunges or bites was
observedinjust22.7% ofthetrialsandthreebehaviorswereidentifiedasaggression-attenuatingmechanisms:
a hug; fleeing, and a postural pattern (POS). Interactions took place in 59.1% of the trials and the pairs
interacted using one or two behavioral patterns (vibratory and/or postural). The vibratory pattern (VIB)
consisted offorelegvibration, palpal drumming, and abdominal pulsation and wasused byboth residentand
intruder opponents. The postural pattern (POS) was used exclusively by resident males and it was similar to
the behavioral pattern of sexually receptive L. gaucho females; in these cases the intruder male responded
using the VIB. In conclusion, the interaction between adult L. gaucho males is usually non-aggressive. The
behaviors described in this study possibly promote group-living and help to explain the gregarious
populations of recluse spiders. Intra-specific sexual mimicry can occur in these interactions, but this
hypothesis requires further investigation.
Keywords: Aggression, gregariousness, male-male interaction, sexual mimicry
Aggression takes place when an animal animal model for the study of aggression-
attacks or threatens an opponent. Findings in attenuating mechanisms. This is the case of
Game Theory have shown that aggressive or the recluse spiders that are generally solitary
agonistic encounters between conspecifics usu- but can aggregate around and inside buildings
ally minimize and/or delay aggression, improv- (Biicherl 1961; Horner & Stewart 1967; Fischer
ing the individual fitness of the opponents & Vasconcellos-Neto 2005; Marques-da-Silva
(Maynard Smith & Price 1973; Maynard Smith et al. 2006).
& Parker 1976; Whitehouse 1997). In male- Individuals of the recluse spider Loxosceles
male spider interactions, some particular char- gaucho Gertsch 1967 (Araneae, Sicariidae) are
acteristics or behaviors can act as aggression- usually solitary in their natural habitat, as in
attenuating mechanisms, such as differences in the Butantan Institute woods (Japyassu et al.
weight (Suter & Keyley 1984) or size (White- 2003). However, like other recluse spiders they
house 1997; Bridge et al. 2000; Taylor & aggregate in manmade environments or in
Jackson 2003), and ritualized behaviors (Lubin disturbed natural habitats. For instance Stropa
1986). Even the presence/absence ofdetermined & Pinhal (2005) found adult L. gaucho aggre-
elements in the contest area can affect oppo- gating in brick piles deposited on the ground;
nent aggressiveness, as shown by Wells (1988) and Stropa (2004) reported that two males of
for male Triteparvula (Bryant 1935) (Araneae, this speciesmay share asmall retreatin thefield
Salticidae), which escalate contests in the during the day. At night, however, males
presence ofa female model. commonly wander searching for females. The
In addition, aggressiveness and tolerance are silk produced by both males and females is
key factors to understand the evolution of easily recognized in the field and is abundant,
social behavior in spiders (see Uetz & Hieber at least in the Botanic Garden from Botucatu,
1997). Most spiders are essentially solitary, but Brazil. The silk covers portions of the spiders’
a few species have different degrees of socia- retreats which are mainly in crevices and the
bility that range from aggregations of individ- cavities of the litter. The web of L. gaucho is
ual webs to cooperative brood care (Aviles thin, white, and irregular and covers the sub-
1997). There are species that exhibit social strate like a thin sheet. L. gaucho also occurs in
plasticity, i.e., that do not display obligatory house yards but there is no evidence that it
social behavior. These species are a primary prefers this habitat (Stropa & Pinhal 2005). It is
493
494 THE JOURNAL OF ARACHNOLOGY
endemicfrom southwestern Brazil and it occurs balance (160 g; 0.01 mg) one day before
mainly in the states of Sao Paulo and Parana experiments. The avg. weight of the specimens
(Marques-da-Silva & Fischer 2005). was 55.23 ± 15.42 mg (mean ± SD). Each
In this study, a resident-intruder paradigm spider was tested only once.
was used to examine interactions between male One week before the encounter, one spider of
L. gaucho in order to study its intrasexual each pair was marked with a nail polish dot on
aggressiveness and to explore the possible the abdomen to facilitate individual recogni-
influences of the male-male interactions on tion. No toxic effects of this product were
the lifestyle of recluse spiders. Voucher speci- observed. Temperature and relative air humid-
mens are deposited at the Colegao de Aranhas ity were kept at approximately 25° C and 70%
do Departamento de Zoologia, UNESP, Cam- inside the arenas.
pus de Botucatu, UBTU. The encounters were tape recorded (VHS
METHODS system) from above the arenas. Each encounter
— ended when a “losing” spider was identified
Test animals and holding conditions. Forty- (e.g., when either one of the opponents ran
four adult male L. gaucho were hand-collected away from the rival or abandoned the in-
from stalk crevices of Eucalyptus sp. at the teraction by moving backwards).
—
Botanic Garden from IB, UNESP, Botucatu, Data analyses, The behavioral sequences
Brazil (22°59'S, 48°26'W). These animals were were qualitatively and quantitatively described
m(8a5inmtaminXed25inmminidnitveirdnuaalldigalmaestser)tefsotr atbuobuets pinatahwfalyosw dthiaatgreanmde(dFigi.n 1a)ggsroestshiaotnbaehnadvinoorna-l
30 days before the experiments, and fed once aggression could be identified. Aggressive
a week on insects collected by sweeping. About behaviors included lunges or bites (Table 1).
3 days before the experiment, the spiders were Encounters without occurrence of these lunges
fed in excess (5 Musca domestica per spider) to or bites were defined as non-aggressive en-
balance satiation level. The forty-four spiders counters. The predominance ofthese aggressive
were used for twe—nty-two pairwise encounters. and non-aggressive encounters was tested using
The encounters. Twenty-two encounters be- the Chi-square goodness-of-fit test with Yates
tween males were carried out using an intruder- correction.
resident paradigm. One spider, designated as
RESULTS
the resident, was placed inside the arena (a
transparent plastic cage, 110 mm diameter X The general pattern of encounters between
70 mm high). This area was about 30-50% male L. gaucho began with the intruders
bigger than the retreats of L. gaucho in the walking into the arena and touching the
field. One week after this, time enough for the residents’ web {n = 21). In one instance, the
resident to spin its irregular web, the external resident moved first. After these first move-
transparent tube (60 mm long X 40 mm di- ments, in all cases, (n = 22), the intruders
ameter) attached to the arena was disconnect- vibrated their body appendices; a pattern des-
ed. Another spider, designated as the intruder, ignated as “VIB” (Table 1 and Fig. 1). Fol-
was introduced in the tube that was recon- lowing this, the residents responded by fleeing
nected to the arena. At this point, both the {n = 9) or interacted usingthe VIB pattern, i.e.,
resident and the intruder were allowed to similar to the intruders’ behavior {n = 8). The
encounter each other. other residents interacted using a postural
Spider pairs were selected in order to balance performance rather than movements, a pattern
the relative weight between the opponents. designated as “POS” {n ~ 5) (Table 1 and
Thus, in 11 encounters weight difference was Fig. 1). The duration of the VIB-VIB encoun-
higher than 10% while in the other 11 ters was of 3-8 min while the duration of the
encounters weight difference was lower than VIB-POS encounters was much longer, 18-
10%. In the trials with either high or low 37 min. In both types ofencounters, the spiders
relative weight, the frequency of residents and of each pair approached and touched each
intruders with higherweight was also balanced, otherwith their forelegs (Fig. 1). With theVIB-
i.e., residents were heavier in five trials and VIB interaction, when the opponents reached
intruders were heavier in the other six trials. the face-to-face position, they overlapped their
Spiders were weighed with a Mettler H20T forelegs (behavior named “hug” -Table 1) and
—
STROPA—MALE-MALE INTERACTION OF LOXOSCELES GAUCHO 495
Intrudermale
(insidethetube) Residentmale
from 16 to 22 trials from4 to 6 trials
from 7 to 9 trials
from 10 to 15 trials from 1 to 3 trials
Figure 1. Flow diagram of the male-male interaction of L. gaucho {n = 22). Dashed lines delimit the
context. Dotted lines indicate the determined behavioral patterns (movements and/or postures of specific
portions ofthe spider’s body). The gray line delimits the period ofaggression (area below it). Thickness of
arrows indicates the frequency with which the behaviors were observed.
one spider ofthe paireither fled orlunged at its abandoned the interaction {n = 3), or fled {n =
opponent. On the other hand, when VIB-POS 2). In these last two cases the interaction was
interaction took place, the intruder advanced longer than 30 min and the residents became
under the resident’s prosoma and then either aggressive, i.e., they changed from POS into
496 THE JOURNAL OF ARACHNOLOGY
—
Table 1. Behavioral patterns and conspicuous behaviors ofthe male-male interaction ofL. gaucho.
Patterns Behaviors Description
VIB Foreleg vibration Simultaneous vertical movement ofthe pairs oflegs whose tarsi
touch the resident’s silk.
Palpal drumming Alternate vertical palp movements
Abdominal pulsation 1 Vertical and horizontal abdomen movements
POS Abdominal pulsation 2 Just vertical movements and slower than the abdominal pulsation 1
Motionless Stop walking
Legs sideways Extension ofall legs sideways
Hug Opponentsoverlaptheirforelegs(opponents’ forelegstouchandbeat
each other)
Lunge One spiderjumps abruptly towards its opponent
Bite Cheliceraeholdapartofthebodyofaspiderandthefangspiercethe
cuticle
VIB pattern and immediately the opponents This is expected because male spiders may not
hugged each other and the residents lunged establish residence in the natural habitat since
against the intruders. they move while searching for females (Foelix
Non-aggressive encounters were preponder- 1982). Moreover, they are not likely to defend
ant (77.3%) (n = 17: x\ = 5.500, P < 0.025). empty territories (e.g., without females or other
Aggression (occurrence oflunges or bites) took resources). The present study indicates that
place in just five encounters (22.7%) (Fig. 1), intruder males were always interested in inter-
always after the VIB-VIB interaction, even actingwith residents displaying theVIB pattern
when the residents started their interaction (Fig. 1). However, this interaction was also
using the POS pattern. In a single aggressive expected since information about habitat qual-
encounter there was physical injury; the injured ity can be obtained from other spiders or
spider autotomized the bitten leg (Fig. 1). simply from silk (Hodge & Storfer-Isser 1997;
Schuck-Paim & Alonso 2001; Bilde et al. 2002).
DISCUSSION
An unexpected aggression-attenuating mech-
The present study indicates that interactions anism observed in this study is the POS pattern
between male L. gaucho are predominantly displayed by five of the 22 residents. In these
non-aggressive, at least in the resident-intruder trials the resident was nearly motionless with
paradigm. When aggression (lunges or bites) the legs stretched sideways, pulsating its abdo-
took place, it occurred only after the hug. But men slower than the intruders, and had its
in this species, the hug does not necessarily prosoma lifted by the intruder advancement.
trigger aggression since it also occurred in non- According to Rinaldi & Stropa (1998), when
aggressive male-male (Fig. 1) and female-fe- female L. gaucho are sexually receptive, they
male encounters (Stropa & Rinaldi 2001). The allow males to lift their prosoma to copulate.
hug is possibly used by adult L. gaucho spiders Males use their own prosoma to lift females,
to evaluate fighting ability and/or the size of such as the intruders did in the present study.
their opponents, allowing for a decision be- This may not be a simple case of mistaken
tween fleeing or fighting. Ifthis is true; the hug sexual identity because there were differences in
is an aggression-attenuating mechanism since it the male-male interaction observed here and
delays aggression and, as a consequence, im- themale-female interaction reported by Rinaldi
proves individual fitness. This situation is and Stropa (1998). Males interact with females
predicted in asymmetric animal contests (May- onlybypalpal drumming, forelegvibration and
nard Smith & Price 1973; Maynard Smith & abdomen pulsation (Rinaldi & Stropa 1998);
Parker 1976; Whitehouse 1997). e.g., the VIB pattern seen here. Female L.
Two more conspicuous aggression-attenuat- gaucho become receptive for mating only by
ing mechanisms were found: the fleeing and the stretching their legs sideways, pulsating their
POS pattern. Residents fled in 9 ofthe 22 trials abdomen slowly and keeping themselves nearly
&
without further interaction with the intruders. motionless (Rinaldi Stropa 1998); i.e., these
STROPA—MALE-MALE INTERACTION OF LOXOSCELES GAUCHO 497
females use only the POS pattern in the sexual infestation in manmade environments where
interaction. In the present study, male L. Loxosceles can become a public health prob-
gaucho used both the VIB and POS patterns lem. However, interaction is only one factor to
in the male-male interaction. be considered and it is certainly linked to other
It is possible that the male intruders were variables such as resource availability and
courting and trying to copulate with the male habitat architecture.
residents as ifthey were receptive females. For
spiders, this may be an instance ofintraspecific ACKNOWLEDGMENTS
sexual mimicry, which is when an animal gets I am grateful to Dr. L. C. Jordao and Dr. B.
some advantage over its conspecific opponent D. Roitberg for valuable criticism and sugges-
by present itself as if it is an individual of the tions on the several drafts ofthis manuscript. I
opposite sex. Further investigation is needed to am also very grateful to the editor Dr. G.
corroborate this hypothesis since only fivecases Stratton and anonymous referees for their
are described in the present study. Sexual
suggestions to improve this paper. This study
mimicry in spiders has been reported only in
was supported by a fellowship to A.A.S. by the
interspecific interactions such as the bolas Fundagao de Amparo a Pesquisa do Estado de
spider Mastophora sp. attracting prey (Eber-
Sao Paulo (FAPESP: 96/09389-0).
hard 1977; Stowe et al. 1987; Yeargan 1994)
and Portiafimbriata Doleschall 1859 mimick-
LITERATURE CITED
ing a male of Euryattus sp. (Salticidae) to
attack the female hiding in a leaf (Jackson & Aviles, L. 1997. Causes and consequences of co-
Wilcox 1990). operation and permanent-sociality in spiders.
useTdhePOtwSofeonlcloouwnetderbsyiVnIwBhiacrhe irnetsriidgeunitngmaalneds iPnp.I4n7se6c^t9s8.anIdn TAhreacEhvnoildustion(J.oCf.SoCchiaoleBe&havBi.oJr.
Crespi, eds.). Cambridge University Press, Cam-
possibly indicate that male L. gaucho has some bridge, UK.
behavioral plasticity. In both cases, the contest Bilde, T., A.A. Markalov, P.W. Taylor & Y. Lubin.
escalated to aggressive behaviors after the 2002. State-dependent decisions in nest site
resident displayed VIB, and the resident won selection by a web-building spider. Animal Be-
the contest. According to Horel et al. (1996), haviour 64:447-452.
behavioral plasticity is a pre-adaptation for Bridge, A.P., R.W. Elwood & J.T.A. Dick. 2000.
social life in spiders since it amplifies the Imperfect assessment and limited information
intraspecific tolerance. This hypothesis may preclude optimal strategies in male-male fights in
explain male pairs of this species sharing theorb-weavingspider Metellinamengei. Proceed-
retreats in the field during the day (Stropa ings of the Royal Society B: Biological Sciences
267:273-279.
2004).
Biicherl, W. 1961. Aranhas do genero Loxosceles e
In conclusion, the intraspecific interaction of
Loxoscelismo na America. Ciencia e Cultura 13:
male L. gaucho in the resident-intruder para-
213-224.
digm is usually non-aggressive. This profile is Eberhard, W.G. 1977. Aggressive chemical mimicry
a result of the three aggression-attenuating by a bolas spider. Science 198:1173-1175.
mechanisms identified: the hug, the fleeing Fischer, M.L. & J. Vasconcellos-Neto. 2005. Micro-
and the POS pattern. These mechanisms may habitats occupied by Loxosceles intermedia and
facilitate group living. Recluse spiders have Loxosceles laeta. Journal ofMedical Entomology
been classified as solitary and territorial (Bii- 42:756-765.
cherl 1961; Weens & Whitcomb 1975; Japyassu Foelix, R.F. 1982. Biology of Spiders. Harvard
et al. 2003), but according to several reports University Press, Cambridge, Massachusetts.
they also live in conspecific aggregations and 306 pp.
infest manmade environments (Biicherl 1961; Hodge, M.A. & A. Storfer-Isser. 1997. Conspecific
Levi & Spielman 1964; Howner & Stewart and heterospecific attraction: a mechanism of
1967; Waldron et al. 1975; Fischer & Vascon- wtieobn-sibtyewseebl-ebcutiiolndilnegadsipnigdertso.aEgtghroelgaotgiyon10f3o:r8m1a5--
cellos-Neto 2005; Marques-da-Silva et al. 826.
2006). The investigation of the causes of these Horel, A., B. Krafft & S. Aron. 1996. Processes de
aggregations might reveal the main factors socialisation et preadaptations comportementales
modulating the lifestyle of recluse spiders and chez les araignees. Bulletin de la Societe Zoologi-
might elucidate mechanisms that minimize que de France 121:31-37.
498 THE JOURNAL OF ARACHNOLOGY
Horner, N.V. & K.W. Stewart. 1967. Life history of Stropa, A.A. 2004. Seiegao de arquitetura de micro-
the brown spider, Loxosceles reclusa Gertsch and habitat pela aranha-marrom Loxosceles gaucho
Mulaik. TheTexasJournalofScience 19:333-347. (Gertsch 1967). Tese de doutorado, Instituto de
Jackson, R.R. & R.S. Wilcox. 1990. Aggressive Biodendas de Botucatu, Universidade Estadual
mimicry, prey-specific predatory behaviour and Paulista, Sao Paulo, Brazil 47 p.
predator-recognition in the predator-prey interac- Stropa, A.A. &D. Pinhal. 2005. Habitatarchitecture
tions of Portia fimbriata and Euryattus sp., affects the aggregation level among adult brown
jumping spiders from Queensland. Behavioral spiders: evidence from a case study. Newsletter of
Ecology and Sociobiology 26:111-119. the British Arachnological Society 104:4-6.
Japyassu, H.F., C.R. Macagnan & L Knysak. 2003. Stropa, A.A. & I.M.P. Rinaldi. 2001. Relative
Eggsac recognition in Loxosceles gaucho (Ara- tolerance and communication in agonistic behav-
neae, Sicariidae) and the evolution of maternal iour between females ofLoxosceles gaucho (Ara-
care in spiders. Journal of Arachnology 31:90- neae, Sicariidae). Bulletin ofthe British Arachno-
104. logical Society 12:41M5.
Levi, H.W. & A. Spielman. 1964. The biology and Suter, R.B. & M. Keyley. 1984. Agonistic interac-
control of the South American brown spider, tions between male Frontinella pyramitela (Ara-
Loxosceles laeta (Nicolet), in a North American neae, Linyphiidae). Behavioral Ecology and So-
focus. American Journal ofTropical Medicine & dobioiogy 15:1-7.
Hygiene 13:132-136. Taylor, P.W. & R.R. Jackson. 2003. Interacting
Lubin, Y.D. 1986. Courtship and alternative mating effects of size and prior injury injumping spider
tactics in a social spider. Journal ofArachnology conflicts. Animal Behaviour 65:787-794.
14:239-257. Uetz, G.W. & G.S. Hieber. 1997. Colonial web-
Marques-da-Silva, E. & M.L. Fischer. 2005, Dis- building spiders: balancing the costs and benefits
tribuigao das especies do genero Loxosceles ofgroup-living. Pp. 458-^75. In The Evolution of
Heinecken &Lowe, 1835 (Araneae; Sicariidae) no Social Behavior in Insects and Arachnids (J.C.
Estado do Parana. Revista da Sociedade Brasi- Choe & B.J. Crespi, eds.). Cambridge University
leira de Medidna Tropical 38:331-335. Press, Cambridge, UK.
Marques-da-Silva, E., R. Souza-Santos, M.L. Waldron, W.G., M.B. Madon & T. Suddarth. 1975.
Fischer & G.B.G. Rubio. 2006. Loxosceles spider Observations on the occurrence and ecology of
bites in the state of Parana, Brazil: 1993-2000. Loxosceles laeta (Araneae, Scytodidae) in Los
Journal of Venomous Animals and Toxins in- Angeles, California. California Vector Views 22:
29-36.
cluding Tropical Diseases 12:110-123.
Maynard Smith,J. &G.A. Parker. 1976. Thelogicof Weens, H.V., Jr. & W.H. Whitcomb. 1975. The
asymmetric contests. Animal Behaviour 24:159- brown recluse spider, Loxosceles reclusa Gertsch
andMulaik(Araneae: Loxoscelidae). Entomology
175.
Maynard Smith, J. & G.R. Price. 1973. The logic of Circular 158. Florida Department of Agriculture
animal conflict. Nature 246:15-18. and Consumer Services, Division of Plant In-
Rinaldi, I.M.P. & A.A. Stropa. 1998. Sexual dustry, Gainesville, Florida. 2 pp.
Wells, M.S. 1988. Effects ofbody size and resource
behaviourinLoxoscelesgauchoGertsch(Araneae,
value on fighting behaviour in a jumping spider.
Sicariidae). Bulletin ofthe British Arachnological
Animal Behaviour 36:321-326.
Society 11:57-61.
Schuck-Paim, C. & W.J. Alonso. 2001. Deciding Whitehouse, M.E.A. 1997. Experience influences
male-male contests in the spider Argyrodes anti-
whereto settle: conspecificattraction andweb site podiana (Theridiidae: Araneae). Animal Behav-
selection in the orb-web spider Nephilengys
iour 53:913-923.
cruentata. Animal Behaviour 62:1007-1012.
Stowe, M.K., J.H. Tumlinson & R.R. Heath. 1987. YeaArngnauna,l KR.eVv.iew19o9f4.EntBoimoloolgoygyo3f9:b8o1l-a9s9. spiders.
Chemicalmimicry: bolas spidersemitcomponents
of moth prey species sex pheromones. Science Manuscript received 26 July 2006, revised 9 August
236:964-967. 2007.