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Nuptial Gift-Giving Behaviour and Male Mating Effort in the Neotropical Spider Paratrechalea Ornata (Trechaleidae)

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Nuptial Gift-Giving Behaviour and Male Mating Effort in the Neotropical Spider Paratrechalea Ornata (Trechaleidae) Animal Behaviour 79 (2010) 1031–1036 Contents lists available at ScienceDirect Animal Behaviour journal homepage: www.elsevier.com/locate/anbehav Nuptial gift-giving behaviour and male mating effort in the Neotropical spider Paratrechalea ornata (Trechaleidae) Marı´a J. Albo *, Fernando G. Costa Laboratorio de Etologı´a, Ecologı´a y Evolucio´n, Instituto de Investigaciones Biolo´gicas Clemente Estable article info The occurrence of nuptial gifts is rare in spiders, being well known only for a single species, Pisaura Article history: mirabilis (Pisauridae), whose males offer females a prey wrapped in silk during courtship. Although some Received 7 October 2009 males can mate without offering a prey, the gift in this species is thought to represent male mating effort. Initial acceptance 25 November 2009 Male gift offering has been recently described in Paratrechalea ornata , a Neotropical spider belonging to Final acceptance 22 January 2010 another family, Trechaleidae. We investigated the function of the gift in this species by testing the mating Available online 12 March 2010 effort hypothesis and two other nonexclusive hypotheses, sexual cannibalism avoidance and paternal MS. number: 09-00623 investment. Two groups of males were exposed to virgin females: 23 males with no prey (NP group) and 21 males carrying a prey (CP group). Mating success, courtship, copulation and first oviposition were Keywords: recorded. Males from group CP had better mating success, longer copulations and longer palpal inser- male mating effort tions than those from NP. Longer copulations were associated with earlier eggsac construction and oviposition acceleration oviposition. Some unmated males from NP wrapped prey carrion when they returned to their breeding Paratrechalea ornata sexual selection jars after the trial. Our findings suggest that nuptial gift giving represents male mating effort for P. ornata . spider nuptial gift Nuptial gifts would allow males to control copulation duration and to accelerate female oviposition, improving sperm supply and paternity, and minimizing possible costs of remating with polyandrous females. Ó 2010 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. Nuptial gifts are common in invertebrates and have been inten- reproductive success (mating effort hypothesis: Thornhill 1976b; sively studied in insects ( Boggs 1995; Vahed 2007; Gwynne 2008 ). In Simmons & Gwynne 1991; Eberhard 1996; Wolfner 1997; Heifetz general, gifts could be prey, carrion or plants, regurgitations, salivary et al. 2001; Arnqvist & Rowe 2005; Sakaluk et al. 2006 ). and glandular secretions, specialized male body parts and ejaculated Two other hypotheses can explain the adaptive significance of substances ( Vahed 1998, 2007 ). Historically, nuptial gifts were nuptial gifts, beyond the paternal investment and mating effort: defined as potentially nutritive substances donated by males to avoidance of sexual cannibalism and sensory exploitation ( Vahed females during mating ( Boggs 1995 ). Such gifts can supply the female 1998, 2007 ). Cannibalism avoidance was proposed by Bristowe with nutrients and so function as paternal investment ( Thornhill (1958) and Kessel (1955) as a tactic to prevent female attacks, but 1976a; Gwynne 1984; Simmons & Parker 1989 ). In some insects has limited empirical support. Sensory exploitation assumes males the nuptial gift has a positive effect on female fecundity and can also manipulate females by offering gifts that exploit pre-existing increase female longevity ( Wiklund et al. 1993; Karlsson 1998; Lewis female sensory biases, without necessarily implying costs for & Cratsley 2008 ). However, because there is limited knowledge of the females (intersexual conflict). A good example is the donation of nutritional value of gifts, and there is evidence that some nuptial gifts spermatophores in crickets, which provide the gustatory stimuli improve male reproductive success but do not provide direct that females prefer (Sakaluk 2000; Vahed 2007 ). These hypotheses (nutritious) benefits for females, sexual conflict between the sexes are not mutually exclusive. could be operating ( Vahed 1998, 2007 ; but see Gwynne 2008 ). By The occurrence of nuptial gifts is rare in spiders; in fact the providing such gifts, males can manipulate the time of copulation, Palaearctic Pisaura mirabilis (Pisauridae) has been the only well- thus promoting the production of large ejaculates, inducing a female studied species, particularly in the context of sexual selection refractory period, accelerating oviposition and maximizing their (Austad & Thornhill 1986; Lang 1996; Drengsgaard & Toft 1999; Stålhandske 2001, 2002; Bruun et al. 2003; Prokop 2006; Bilde et al. 2006, 2007; Andersen et al. 2008; Hansen et al. 2008; Prokop & Maxwell 2009 ). Males of this species offer females * Correspondence: M. J. Albo, Laboratorio de Etologı´a, Ecologı´a y Evolucio ´ n, a prey wrapped in silk during courtship, which is bitten and Instituto de Investigaciones Biolo ´ gicas Clemente Estable, Av. Italia 3318, 11600 Montevideo, Uruguay. consumed by the female during mating. Stålhandske (2001) E-mail address: [email protected] (M.J. Albo). observed that in a Scandinavian population, males lacking 0003-3472/$38.00 Ó 2010 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.anbehav.2010.01.018 1032 M.J. Albo, F.G. Costa / Animal Behaviour 79 (2010) 1031–1036 a donation can also mate without risk of cannibalism. She sug- (Fig. 1). The ambient temperature during the experimental period gested that the gift facilitates the copulation position, and keeps the was 20.4 Æ 2.3 C. female occupied handling it during mating. Larger gifts result in To investigate the function of the nuptial gift in courtship and longer copulations and more fertilized eggs ( Austad & Thornhill mating, we exposed 23 females to a male with no prey (group NP) 1986; Stålhandske 2001 ). In P. mirabilis the gift functions as male and 25 females to a male carrying a prey (group CP). One day before mating effort to facilitate copulations, and the silk wrapping the experimental trial, a female was placed into the experimental provides direct benefits to males in the form of increased control cage allowing silk deposition and habituation, whereas an adult over mating and longer copulations ( Lang 1996; Stålhandske 2001; male was placed in a petri dish and fed with a fruit fly ( Drosophila Bilde et al. 2007; Andersen et al. 2008 ). sp.) to prevent starvation. For the mating trials, each male of the CP Recently, Costa-Schmidt et al. (2008) described that in Para- group received a large living fruit fly ( Drosophila funebris) and was trechalea ornata , a Neotropical spider that belongs to the family transferred to the female experimental cage immediately after he Trechaleidae, males also construct and donate nuptial gifts during captured the prey. In both treatments the trials consisted of two courtship and copulation. Paratrechalea ornata is found in southern steps. First, we exposed the male to the female silk, isolated from Brazil, northern Argentina, Paraguay and Uruguay ( Carico 2005 ) the female by an opaque glass barrier. Second, after 15 min we and, like other trechaleids, inhabit semiaquatic environments, carefully removed the barrier, allowing male–female encounter. especially the borders of streams and rivers. Females carry the This time period is enough for males to wrap the prey in silk ( Albo eggsac attached to the spinnerets, similar to the wolf spiders et al. 2009 ). If a male did not wrap the prey, we allowed the male to (Lycosidae). In Uruguay P. ornata co-occurs with other larger encounter the female carrying the unwrapped prey. Therefore, trechaleid species such as Trechalea bucculenta and Trechaleoides males from the CP treatment could encounter females carrying biocellata (M. J. Albo & F. G. Costa, unpublished data). As was found either a wrapped or an unwrapped prey. If the male courted in the pisaurid P. mirabilis , males of P. ornata may present either a female with a prey but mated without donating it (maintaining a wrapped or an unwrapped nuptial prey gift ( Albo et al. 2009 ). the prey in his chelicerae), we included these data in CP for the Prey wrapping seems to be triggered by perception of cues on the courtship analyses, but considered them as a separate group (no female’s silk and increases in frequency according to the male’s age donation, ND) for the mating analyses. (Albo et al. 2009 ). Individuals were not reused, except for three females that were In the present study we tested the function of the nuptial gift in first used in NP and did not mate, and were subsequently reused in CP. P. ornata by comparing the sexual behaviour and the reproductive To avoid possible effects of previous experience, we excluded their success of pairs in both the presence and the absence of a nuptial data from the courtship analysis, but we included them in the mating gift. Under the male mating effort hypothesis, males presenting analysis because of their virgin condition. Each trial was stopped a nuptial gift are predicted to experience briefer courtship, higher when the mating ended, or after 30 min when no interactions were mating success and longer mating than males without a gift. Under observed. Behaviours and interactions between individuals were the paternal investment hypothesis, females that received a nuptial timed and recorded. We noted the occurrence of prey wrapping,
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