Mechanisms underlying egg-sac opening
in the subsocial spider Anelosimus cf. studiosus (Araneae Theridiidae)
C
. Viera 1,2,3, S. Ghione 1,2 and F.G. Costa 1
1 Laboratorio de Etología, Ecología y Evolución, IIBCE, Av. Italia 3318, 11600 Montevideo, Uruguay
2 Sección Entomología, Facultad de Ciencias, Iguá 4225, 11400 Montevideo, Uruguay
Received 14 June 2006, accepted 11 October 2006
Extended maternal care is one of the first steps towards sociality in spiders.
Females of Anelosimus cf. studiosus care for their egg-sacs and open them to allow the emergence of the spiderlings, which they feed by regurgitation. In this paper we studied the mechanisms underlying egg-sac opening behaviour in this subsocial spider, by exchanging egg-sacs with different degrees of maturation between two groups of females. We also maintained isolated egg-sacs to test the ability of the spiderlings to emerge by themselves. Mothers always cared for the foreign egg-sacs because they were unable to recognize their own egg-sac. Egg-sac opening by foster mothers matched the timing at which the mothers would have opened their own egg-sacs. All the mothers ate eggs, but not larvae or nymphs. Spiderlings were unable to emerge by themselves. The timing of egg-sac opening seemed to depend mainly on an internal factor within the mother, but the exact moment of opening appeared to be adjusted by external stimuli generated
inside the egg-sac (nymphal movements). Hence, because material factors rather than nynphal moviments are the major stimulers for egg-sac opening, this species would be unable to care for foreign egg-sacs making communal egg-sac care impossible and thus constraining evolution towards more social behaviour.
k
ey words: Anelosimus, sub-social spiders, experimental egg-sac exchange, egg-sac opening.
Introduction . . . . . . . . . . . . . . . . . 62
Materials and methods . . . . . . . . . . . . . . 63
Results . . . . . . . . . . . . . . . . . . 64
Discussion . . . . . . . . . . . . . . . . . 65
Acknowledgements . . . . . . . . . . . . . . . 66
References . . . . . . . . . . . . . . . . . 66
Ethology Ecology & Evolution 19: 61-67, 2007
3 Author for correspondence: Carmen Viera (E-mail: cviera@fcien.edu.uy).
62
C. Viera, S. Ghione and F.G. Costa
INTRODUCTION
Parental care is the first step towards sociality in spiders, because the mother
with her offspring is the basic nucleus of a social group. Delaying brood care and mutual tolerance among offspring allow an extended life in groups (Buskirk 1981). Tolerance among adults and cooperative brood care are another evolutionary steps toward high levels of sociality, as is well-known in social insects. In spite of the advantages of living in groups, most spiders are typically solitary; in fact, only about 23 among more than 38,000 known species can be considered social (Whitehouse
& Lubin 2005). Mutual aggressiveness is avoided or minimized throughout the consecutive juvenile instars, allowing a permanent association among individuals.
Hence, mutual tolerance is an early requirement which has to be achieved on the way from solitary to social spiders (Kullman 1972). Consequently, it is not surprising
that extended parental care or relatively permanent social groupings are present in few spider species (Buskirk 1981).
Social behaviour in spiders involves cooperation in nest building, web maintenance,
prey capture, feeding and brood care (Avilés 1997) and it is largely governed by the foraging function rather than by the reproductive function, as in insects (Whitehouse & Lubin 2005). Social spiders (non-territorial permanent social, sensu Avilés 1997) show a highly female-biased sex ratio (Vollrath 1986, Avilés & Maddison
1991, Vasconcellos-Neto et al. 1995, Avilés 1997) increasing the amount of the sex that conduct the required tasks. Maternal care efforts are shared by a group of females (Avilés 1997), but the spiders differ from social insects because all adult females are potentially able to reproduce (however, see Vollrath 1986, Henschel et al. 1995, Vasconcellos-Neto et al. 1995, Schneider 2002). In subsocial spiders (non-territorial, periodic-social spiders, sensu Avilés 1997), adult females leave the colony after maturation and do not cooperate in brood care (Brach 1977; Furey 1995, 1998; Jones & Parker 2002). Hence intolerance among adult females would be the main limitation for advancing towards sociality (Brach 1977; Avilés 1997; Viera et al. 2002, in press a).
The theridiid genus Anelosimus (Simon 1891) includes several solitary, subsocial
and social species distributed in temperate and tropical areas, which makes it a good model for studying the evolution of social systems in spiders. Anelosimus cf. studiosus is a subsocial species inhabiting Uruguay, which is closely related to the Northern A. studiosus (I. Agnarsson in litt.). Anelosimus cf. studiosus shows a 2:1 sex ratio biased towards females (Viera et al. 2002, in press a). Adult females usually do not tolerate each other, hence they disperse on reaching adulthood, and founding new colonies (Viera & Albo 2001). However in the field nests occur that are inhabited by several females, the so-called multi-female nests, in which daughters
remain at mother’s nest but each maintains an individual territory (Viera 2005, Viera et al. in press a). Ghione et al. (2003) and Viera et al. (in press b) found that two instars, prelarva and larva, develop inside A. cf. studiosus egg-sacs 17-18 days after egg laying, and the larva moults 3 days later to become the first nymph, emerging immediately afterwards (day 21 after oviposition). The female takes care for her own egg-sac throughout development (Viera et al. 2003, in press a) and opens the ripe egg-sac by making a large hole (1.3 mm diameter) to allow the emergence
of the nymphs (Ghione et al. 2003, Viera et al. in press a, in press b). A mean of 30 spiderlings emerge from each egg-sac (Viera et al. in press a).
This is the first study of the factors underlying egg-sac opening in subsocial spiders,
and its implications for cooperative brood care. In solitary spiders, Eason (1964)
63
Egg-sac opening in a subsocial spider
found in Pardosa lapidicina (Lycosidae) that egg-sac opening depends on micro-movements
inside the egg-sac which elicit opening by the mother. However, in some other lycosid species of the genus Trochosa, stimuli from the egg-sac did not causes opening
by the mother. Instead, the mother has a neuro-endocrine mechanism that determines
egg-sac opening (Engelhardt 1964). On the other hand, Fujii (1978) in Pardosa astrigera and Vannini et al. (1986) in Pardosa hortensis suggested that the mechanism underlying egg-sac opening behaviour could be a combination of both internal and external mechanisms, which would act together inducing the mother to open the sac at the right moment of spiderling development.
In this paper we experimentally investigated which mechanisms are involved in egg-sac opening behaviour in Anelosimus cf. studiosus, by testing possible internal
and external factors. Additionally, we discuss how these mechanisms could be implicated in the evolution of sociality in spiders.
MATERIALS AND METHODS
Females were raised under laboratory conditions in groups from new-born spiderling instars until the penultimate instars were reached. They were maintained in petri dishes (9 cm diameter, 1 cm height) and provided with living flies (mainly Drosophila spp. and Musca spp.) as food. Their mothers were captured from three different populations in Uruguay. Juveniles that reached the penultimate instar were individually raised until adulthood in small petri dishes (3.5 cm diameter, 0.9 cm height). Virgin adult females were mated once and controlled
daily for construction, consumption or abandon of the egg-sacs. During the experimental period the room temperature averaged 24 °C (range 22-26).
Tests of egg-sacs exchanges were conducted with two experimental groups. In Group A, 27 “old” egg-sacs (mean 17.7 ± 1.6 SD days since oviposition) were removed from 27 females which were immediately provided with a “new” egg-sac (mean 5.1 ± 3.4 SD days since oviposition)
that had been removed from 27 females belonging to Group B. In Group B, 27 females received the “old” egg-sacs as a substitute for their own “new” egg-sacs (Fig. 1).
Additionally, we tested the possibility that the nymphs could emerge from the egg-sacs by themselves. Eight “old” egg-sacs were removed from their mothers and isolated for 10 days
Fig. 1. — Egg-sac exchange experiment between two groups of females with different degree of maturation
of their egg-sacs (18 days after egg laying in females from Group A and 5 days after egg laying
in females from Group B).
Egg-sacexchange18daysEgglaying1day5daysEgglaying1dayGroupAGroupB
64 C. Viera, S. Ghione and F.G. Costa
in small petri dishes (3.5 cm diameter and 0.9 cm height), with a wet cotton. As controls, 9 females were maintained with their own egg-sacs until the emergence of the spiderlings.
RESULTS
All females cared for the foreign egg-sacs. Females from group A opened the foreign egg-sacs 24.1 ± 2.9 SD days after their own egg laying. Twelve females of this group ate eggs, 14 females did not eat eggs but remained near the opened egg-sac, and one female found larvae inside the egg-sac but did not eat them. Females from group B did not clearly open the foreign egg-sacs by making a large hole; instead, a few nymphs (11.0 ± 10.1) emerged through small holes (approximately 0.5 mm diameter) in 17 cases, 25.4 ± 3.2 SD days after the egg laying. Females abandoned these egg-sacs. All of the remaining spiderlings were found dead inside the egg-sacs when opened by the authors. Females tolerated the nymphs in all cases, but they were never seen actively feeding the juveniles with regurgitation as a part of maternal care. These results are summarized in Table 1.
Not a single juvenile emerged from the isolated egg-sacs. However, some very small holes (approximately 0.1 mm diameter) were observed in all of them. Females from the control group successfully opened the egg-sacs by making a large hole, 20.8 ± 3.6 SD days after the egg laying.
The period of time until female egg-sac opening differed significantly between group A and the control group (t = 2.49, P < 0.02). We also found significant differences
in the period of time until juvenile emergence between group B and the control
group (t = 3.22, P < 0.01).
Table 1.
Characteristics of egg-sac opening, spiderling emergence and egg-sac content in the experimental groups.
Experimental condition
Egg-sac opening by the female
Egg-sac wall
Emerged spiderlings
Egg-sac content
Group A (n = 27)
24.1 ± 2.9 days after their own oviposition
One large hole
None
Eggs, some living larvae
Group B (n = 27)
No evidence
Small holes
Few, 25.4 ± 3.2 days after their own oviposition
Spiderlings, majority dead
Isolated egg-sac
(n = 8)
Not applicable
Very small holes
None
Dead spiderlings
Mother with her
egg-sac (n = 9)
20.8 ± 3.6 days after oviposition
One large hole
Numerous
Living spiderlings
Egg-sac opening in a subsocial spider 65
DISCUSSION
The results indicate that females from A. cf. studiosus do not recognize their own egg-sacs, because all of them cared the foreign ones. In fact, very few spider species are capable of recognizing their own egg-sacs although the salticid Portia
labiata (Clark & Jackson 1994) and the sicariid Loxosceles gaucho (Japyassú et al. 2003) are exceptions. This ability could be costly in a social spider such as the eresid Stegodyphus dumicola, where many egg-sacs co-occur (Kürpick 2002) and are gathered together, as also happens in Anelosimus rupununi (Avilés & Salazar 1999). The co-occurrence of egg-sacs is also a possible scenario for Anelosimus cf. studiosus
in multi-females nests. Moreover, we observed experimentally that females with egg-sacs can accumulate foreign egg-sacs (unpublished data).
Nymphs were unable to emerge by themselves from the isolated egg-sacs, in agreement with observations in S. dumicola (Kürpick 2002). Juvenile emergence depends on the mother tearing open the egg-sac at the appropriate moment. The mechanism underlying egg-sac opening seemed to be determined more by internal than external stimuli, according to Engelhardt (1964) for lycosid spiders. In our study, females from Group A opened the foreign “new” egg-sacs 24 days after their own oviposition, i.e. only 3 days after the time (21 days) at which they would have opened their own egg-sacs, according to the control group and to observations by Ghione et al. (2003) and Viera et al. (in press b). This delay of 3 days could be due to the absence of stimuli (nymphal movements) from inside the egg-sac, suggesting that these stimuli are crucial in determining the exact timing of egg-sac opening, which is in agreement with findings for lycosid species Eason (1964).
It would appear that females from Anelosimus cf. studiosus are capable of responding to larval or nymphal movements inside the egg-sac, but only during a brief period or “window” determined by their own biorhythm. Viera et al. (in press b) raised both isolated eggs and mothers with their own egg-sacs and found a synchronization
between the time of moulting to first nymphs and the mothers’ opening
behaviour, suggesting nymph movements prompt the mothers’ to open their egg-sacs. However, females from Group B opened the egg-sacs only partially, in spite of nymphal movements, indicating that these stimuli are not the unique ones, nor the most important for eliciting mother opening behaviour. The holes observed in the “old egg-sacs” (Group B) cannot be attributed to action by the spiderlings alone, because these holes were larger than those observed in isolated egg-sacs, suggesting action by the female. Hence, the females must contribute to making the holes, but certainly not to helping the nymphs emerge, because there were many dead spiderlings
inside egg-sacs of this group. Females from Group B were not able to respond to “premature” nymphal stimuli by making a large hole, but probably chewed the egg-sacs. Other apertures caused by endogenous stimuli were not observed, because females abandoned these egg-sacs.
Females cannibalised many eggs but not larvae or nymphs, suggesting a strong inhibition and high tolerance towards motile instars inside the egg-sac. Krafffft & Horel (1980) argue that the tolerance exhibited by a female spider towards her offspring implies at least two mechanisms: inhibition of predatory behaviour in response to the movements of a distant offspring, and inhibition of cannibalism when in contact with an offspring. This last mechanism would be acting in the presence of the foreign spiderlings. It was particularly interesting that female inhibition
included larvae, an earlier instar of development which presents very little mobility and a different body surface (hairs, spines) compared to the first nymph.
66 C. Viera, S. Ghione and F.G. Costa
In more social species, we suggest that the endogenous mechanism responsible
for the opening of the egg-sac could have been overcome, allowing egg-sac opening by any female other than the mother. This putative mechanism would permit
female cooperative breeding, being a more towards high sociality levels (see Riechert & Jones 2001). Furthermore, more delicate abilities would evolve for detecting stimuli inside the egg-sacs, thus allowing any adult female to adjust to a correct timing of the egg-sac opening from any adult female.
Recapitulating, we found that both factors suggested by Fujii (1978) and Vannini
et al. (1986) — nymphal movements and neuroendocrinal mechanisms in the mother — determine the timing of egg-sac opening in Anelosimus cf. studiosus female. The synchronization and adjustment between these factors permit the input of key stimuli through a narrow window period, constraining evolution to more social levels.
ACKNOWLEDGEMENTS
We thank Anita Aisenberg, who critically read the manuscript and improved the English.
We also acknowledge the editors and two anonymous reviewers for their assistance and corrections, which improving the final manuscript.
REFERENCES
A
vilés L. 1997. Causes and consequences of cooperation and permanent-sociality in spiders, pp. 476-498. In: Choe J. & Crespi B., Edits. The evolution of social behavior in insects and arachnids. Cambridge: Cambridge University Press.
A
vilés L. & Maddddison W.P. 1991. When is the sex ratio biases in social spiders?: chromosome studies of embryos and male meiosis in Anelosimus species (Araneae, Theridiidae). Journal of Arachnology 19: 126-135.
A
vilés L. & Salazar P. 1999. Notes on the social structure, life cycle, and behavior of Anelosimus rupununi. Journal of Arachnology 27: 497-502.
B
rach V. 1977. Anelosimus studiosus (Araneae: Theridiidae) and the evolution of quasisociality
in theridiid spiders. Evolution 31: 154-161.
B
uskirk R.E. 1981. Sociality in the Arachnida, pp. 281-367. In: Hermann H.R., Edit. Social insects. Vol. II. New York: Academic Press.
C
lark R.J. & Jackson R.R. 1994. Portia labiata, a cannibalistic jumping spider, discriminates between own and foreign eggsacs. International Journal of Comparative Psychology 7 (1): 38-43.
E
ason R. 1964. Maternal care as exhibited by wolf spider. Proceedings of the Arkansas Academy
of Science 18: 13-19.
E
ngelhardt W. 1964. Die mitteleuropaischen Arten der Gattung Trochosa C.L. Koch, 1848 (Araneae, Lycosidae). Morfologie, Chemotaxanomie, Biologie, Autokologie. Zeitschrift für Morphologie und Ökologie der Tiere 54: 219-392.
Fujii Y. 1978. Examination of the maternal care of cocoon in Pardosa astrigera L. Koch (Araneae,
Lycosidae). Bulletin of the Nippon Dental University, General Education 7: 223-230.
Furey R.E. 1995. Group size and social behavior in a temperate spider, Anelosimus studiosus (Araneae: Theridiidae). PhD Thesis, University of Tennessee, TN, USA, 185 pp.
Furey R.E. 1998. Two cooperative social populations of the theridiid spider Anelosimus studiosus
in a temperate region. Animal Behaviour 55: 727-735.
Egg-sac opening in a subsocial spider 67
G
hione S., Viera C., Nieto F. & Costa F. G. 2003. Desarrollo intraooteca de la araña social Anelosimus studiosus (Araneae, Theridiidae) de Uruguay. Actas VII Jornadas de Zoología del Uruguay: 60.
H
enschel J.R., Lubin Y.D. & Schneider J. 1995. Sexual competition in an inbreeding social spider, Stegodyphus dumicola (Araneae: Eresidae). Insectes Sociaux 42: 419-426.
Japyassú H.F., Macagnan C.R. & Knysak I. 2003. Eggsac recognition in Loxosceles gaucho (Araneae, Sicariidae) and the evolution of maternal care in spiders. Journal of Arachnology
31: 90-104.
Jones T.C. & Parker G. 2002. Delayed juvenile dispersal benefits both mother and offspring in the cooperative spider Anelosimus studiosus (Araneae: Theridiidae). Behavioral Ecology 13: 142-148.
Krafffft B. & Horel A. 1980. Comportement maternal et relations mères-jeunes chez les araignées. Reproduction Nutrition Développement 20 (3B): 747-758.
Kullman E.J. 1972. Evolution of social behavior in spiders (Araneae; Eresidae and Theridiidae).
American Zoologist 12: 419-426.
Kürpick S.M. 2002. Cocoon care in the social spider Stegodyphus dumicola (Eresidae). Proceedings
of the 19th European Colloquium of Arachnology: 39-44.
R
iechert S.E. & Jones T.C. 2001. An aunting model explains increased sociality with increased latitude in Anelosimus studiosus. Abstracts XV International Congress of Arachnology,
South Africa: 141.
S
chneider J.M. 2002. Reproductive state and care giving in Stegodyphus (Araneae: Eresidae) and the implications for the evolution of sociality. Animal Behaviour 63: 649-658.
V
annini M., Contini-Bonacossi B. & Ugolini A. 1986. Cocoon care in Pardosa hortensis (Araneae,
Lycosidae). Biology of Behaviour 11: 85-96.
V
asconcellos-Neto J., Souza A.L.T., Marques E.S.A. & Ferraz F.F.F. 1995. Comportamento social de Anelosimus eximius (Theridiidae: Araneae). Anais de Etologia 13: 217-230.
V
iera C. 2005. Territorialismo en hembras adultas de Anelosimus studiosus (Araneae, Theridiidae)
en condiciones experimentales. Actas del Primer Congreso Latinoamericano de Aracnología: 217.
V
iera C. & Albo M.J. 2001. Interacciones sexuales de una araña social: Anelosimus studiosus (Araneae, Theridiidae). Actas VI Jornadas de Zoología del Uruguay: 69.
V
iera C., Benamú M.A. & Costa F.G. 2002. Fenología y desarrollo de la araña social Anelosimus studiosus (Araneae, Theridiidae) en Uruguay. Actas III Encuentro de Aracnólogos
del Cono Sur, Córdoba, Argentina: 64.
V
iera C., Costa F.G., Ghione S. & Benamú-Pino M.A. (in press a). Progeny, development and phenology of the sub-social spider Anelosimus studiosus (Araneae, Theridiidae) in Uruguay.
Studies on Neotropical Fauna and Environment.
V
iera C., Ghione S. & Costa F.G. 2003. Biorritmos y estímulos intraooteca determinan el cuidado
maternal en Anelosimus studiosus (Theridiidae), una araña social de Uruguay. Resumos do IV Encontro de Aracnólogos do Cone Sul, Sao Pedro (SP), Brasil: 220.
V
iera C., Ghione S. & Costa F.G. (in press b). Post-embryonic development of the sub-social spider Anelosimus cf. studiosus (Araneae, Theridiidae). Bulletin of the British Arachnological
Society.
V
ollrath F. 1986. Eusociality and extraordinary sex ratios in the spider Anelosimus eximius (Araneae: Theridiidae). Behavioral Ecology and Sociobiology 18: 283-287.
W
hitehouse M.E.A. & Lubin Y. 2005. The functions of societies and the evolution of group living:
spider societies as a test case. Biological Reviews 80: 347-361.
