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Sexual Behavior, Cannibalism, and Mating Plugs As Sticky Traps in the Orb Weaver Spider Leucauge Argyra (Tetragnathidae)

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Sexual Behavior, Cannibalism, and Mating Plugs As Sticky Traps in the Orb Weaver Spider Leucauge Argyra (Tetragnathidae) Sexual behavior, cannibalism, and mating plugs as sticky traps in the orb weaver spider Leucauge argyra (Tetragnathidae) Anita Aisenberg & Gilbert Barrantes Naturwissenschaften The Science of Nature ISSN 0028-1042 Volume 98 Number 7 Naturwissenschaften (2011) 98:605-613 DOI 10.1007/s00114-011-0807- y 1 23 Your article is protected by copyright and all rights are held exclusively by Springer- Verlag. This e-offprint is for personal use only and shall not be self-archived in electronic repositories. If you wish to self-archive your work, please use the accepted author’s version for posting to your own website or your institution’s repository. You may further deposit the accepted author’s version on a funder’s repository at a funder’s request, provided it is not made publicly available until 12 months after publication. 1 23 Author's personal copy Naturwissenschaften (2011) 98:605–613 DOI 10.1007/s00114-011-0807-y ORIGINAL PAPER Sexual behavior, cannibalism, and mating plugs as sticky traps in the orb weaver spider Leucauge argyra (Tetragnathidae) Anita Aisenberg & Gilbert Barrantes Received: 5 April 2011 /Revised: 6 May 2011 /Accepted: 7 May 2011 /Published online: 24 May 2011 # Springer-Verlag 2011 Abstract Unpublished field observations in Leucauge seem to determine copulation duration by altering the argyra, a tropical orb weaver spider, suggest the occurrence timing of mating plug formation and through sexual of conspicuous mating plugs that could reduce or prevent cannibalism. This is the first case reported of a mating remating attempts. Otherwise, the sexual behavior of this plug as a sticky trap for males. species remains unknown. The aims of this study were to describe the courtship behavior and copulation in L. argyra Keywords Genital plug . Plug removal . Sexual and investigate mating plug formation in this species. cannibalism . Sexual selection Fourteen virgin females and 12 plugged females were exposed to up to three males and checked for mating plug formation. Of the 12 virgins that copulated, nine produced Introduction plugs (five immediately after copulation), and the five plugged females that copulated produced another mating Mating plugs are widespread in various animal taxa, from plug immediately after copulation. We did not detect the insects and arachnids to reptiles, birds, and mammals transfer of any male substance during copulation but (Drummond 1984; Andrade 1996; Gomiendo et al. 1998; observed a whitish liquid emerging from female genital Knoflach 1998; Wigby and Chapman 2004;Simmons ducts. Plug formation was positively associated with male 2001; Mattoni and Peretti 2004; Aisenberg and Eberhard twanging during courtship. One virgin and four plugged 2009; Leonard and Córdoba-Aguilar 2010; Uhl et al. 2010). females cannibalized males. In seven trials with virgins and These plugs are composed by sperm, glandular products, in three trials with plugged females, the male’s palp adhered parts of spermatophores or male genitalia, and in some to a substance that emerged from female genital ducts and cases the male’s entire body that remains attached to female spread on her genital plate. The male had to struggle genitalia (Uhl et al. 2010). Mating plugs are thought to energetically to free his glued palp; two of these males were function primarily to prevent or minimize female future cannibalized while trying to release their palps. Females mating attempts and consequently, favor the paternity of the copulating male. However, plugs could also have other functions presumably beneficial to females as prevent sperm Communicated by: Sven Thatje desiccation or minimize sperm loss (Boorman and Parker A. Aisenberg (*) 1976;Huber1995, 2005; Simmons 2001; Uhl et al. 2010). Laboratorio de Etología, Ecología y Evolución, Though most mating plugs consist of parts of male Instituto de Investigaciones Biológicas Clemente Estable, genitalia or substances transferred by males, in some cases Av. Italia 3318, CP 11600 Montevideo, Uruguay they are formed by a mixture of female and male e-mail: [email protected] transferred substances or exclusively by female substances (Méndez 2004; Uhl et al. 2010). In the orb-weaving spider G. Barrantes Leucauge mariana (Keyserling 1881) (Tetragnathidae), Escuela de Biología, Universidad de Costa Rica, Ciudad Universitaria, substances transferred by both sexes are necessary to San José, Costa Rica compose an efficient mating plug (Eberhard and Huber Author's personal copy 606 Naturwissenschaften (2011) 98:605–613 1998;Méndez2004; Aisenberg and Eberhard 2009). Larger with L. mariana (Eberhard et al. 1993). We obtained virgin numbers of short male genital insertions and of rhythmic adult females by allowing penultimate females to molt in pushes of the male’s front legs against female’slegsduring captivity. Each penultimate female was maintained in a copulation are associated with a higher probability of female cylindrical glass jar (5–10 cm diameter and 8 cm height) supplying her substance and efficient plug formation in this covered with a thin mesh lid and was monitored everyday species (Aisenberg and Eberhard 2009). This was the first to record molting occurrence. Each jar was provided with a description of female participation in mating plug formation piece of wet cotton and two small branches with leaves. as a possible mechanism of cryptic female choice based on After molting to maturity, each virgin female (n=14) and female selection on the basis of male copulatory courtship. each female collected at the field with a complete genital The genus Leucauge White 1841 comprises more than plug (n=12) was placed on a glass terrarium of 30 cm 100 spider species, but sexual behavior has been studied in length, 16 cm width, and 20 cm height. We attached a only few species (Eberhard and Huber 1998). Male cardboard horizontal frame near the top as substrate for web copulatory courtship seems to be widespread in this genus construction and placed a small plant inside the terrarium to (Eberhard 1994; Castro 1995; Eberhard and Huber 1998) provide humidity and an additional substrate for construc- and mating plugs have been observed at least in three tion of the web. Spiders were offered a prey three times a species: L. mariana, Leucauge venusta (Walckenaer 1841) week: a Tenebrio molitor larvae (Tenebrionidae) or an adult and Leucauge argyra (Walckenaer 1841) (Castro 1995; fly (Sarcophagidae or Calliphorideae). The plants were Eberhard and Huber 1998). Cheliceral clasping between sprayed everyday with water. sexes prior to copulation also occurs in these three Between 1 and 5 days after the female molted to Leucauge species, though it is absent or varies (males seize maturity or 5 days after an adult female with a genital plug female chelicerae) in other species of Tetragnathidae had been captured, each female was exposed to one male (Eberhard 1994; Castro 1995; Eberhard and Huber 1998; that was placed on the border of the orb web. If the female Aisenberg and Eberhard 2009; Aisenberg 2009). Spiders of did not mate after 30 min of male courtship, she was this genus are thus interesting for studies of sperm exposed to a second male within 1 h and then to a third competition, female choice, and the evolution of mating male if the second was not accepted. Females that rejected strategies. three consecutive males were discarded. If spiders courted L. argyra is an orb-weaving spider that constructs but did not copulate, we ended the trial when one spider approximately horizontal orb webs in lowland wet areas abandoned the terrarium, when both spiders remained in Costa Rica (Eberhard 2001). In some sites, this species is motionless for 15 min, or when the female attacked and extremely abundant year round and during the rainy season injured the male or cannibalized him. For determining males are frequently observed guarding penultimate female periods of experimentation, we followed previous studies close to molt (W.G. Eberhard, G. Barrantes and A. on L. mariana (Aisenberg 2009; Aisenberg and Eberhard Aisenberg, unpublished data). Unpublished field observa- 2009) and preliminary observations on the study species. tions show that females of this species have conspicuous Individuals were used once and were randomly assigned mating plugs largely covering their epigyna; their sexual to each trial. The temperature during the trials averaged behavior, however, is unknown. The objectives of this 24.44±1.46°C, range: 21–26. The arena was illuminated study were to describe courtship and copulation in L. with a fiber optic lamp and all trials were recorded with a argyra and investigate mating plug formation in this SONY DCR TRV50 digital video camera (SONY, San species. Additionally, we tested whether plug production Diego, CA, USA) equipped with +4 close-up lenses. is related to female and/or male sexual behavior and tried to Immediately after copulation, each female was observed elucidate the effectiveness of genital plugs in preventing and photographed under a Wild model M3Z dissecting female rematings. microscope (Wild Company, New York, USA), to check for mating plug occurrence, and was checked again 24 h later. All plugged females were inspected before the expositions Materials and methods and after copulation to check if mating plugs were intact or presented slits. Partial plugs were those mating plugs that We collected 14 penultimate females, 12 adult females with covered only part of female epigynum, in contrast to genital plugs that covered entirely their epigynum, and 35 complete plugs that covered both
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