Sensory exploitation of female foraging behavior: Male nuptial gifts in the family Pisauridae

Nuptial gift giving has been investigated in a number of invertebrate species, most namely spiders. In this behavior, males present females with prey items in which females will often accept and feed on. While females feed on the prey, males attempt to mate with them. Based on nutritive benefits for females and increased mating opportunities and copulation success in males, the courtship behavior seems mutually beneficial. There also appear to be protective effects for the males, as demonstrated by decreased levels of attacks and cannibalism by females who accept the nuptial gift (‘shield effect’). This behavior has been studied extensively in the family, Pisauridae, and it varies in occurrence across the clade. Despite this, its function in female mate attraction is not relatively well known. One proposed hypothesis is that it exploits the sensory system of females by imitating signals that are attractive to females (e.g. olfactory cues of stressed or dead prey). If this were the case, then females of a species in which this signal does not occur in the courtship repertoire of male conspecifics and who are positioned early in the clade would accept prey gifts from males of a divergent species. This study investigated whether female, Cladyenis insignis (a non-gift giving species) will accept gifts from and readily mate with male, Pisaura mirabilis (a more recent species that includes gift-giving in its courtship repertoire).

Spider courtship across the family, Pisauridae, involves initial deposition of silk threads by the female. This stimulates the male who then approaches the female with vibrating abdomen, forelegs, and pedipalps. During this time, certain species present a prey-gift while others do not. The female then tends to jump at the male (‘attacks’) who will either choose to flee or face the female for copulation. If the female accepts the male, then the attacks cease and the male inserts his pedipalps into the female epigyne, which consists of two mating ducts that lead from the spermanthecae to the oviduct. The male transfers sperm into each duct one at a time. Thus, at least two insertions are essential to provide sperm to both spermanthecae, highlighting the importance of copulation duration. On rare occasions, the female will cannibalize the male, which explains males’ choice to flee in response to an attack.

Maria Albo et al. (2017) demonstrated that C. insignis still accept gifts from and mate with heterospecific males. Furthermore, the durations of heterospecific matings were much longer than conspecific matings (1 minute vs. 45-50 minutes). While this may be a product of pre-zygotic barriers resulting in reproductive isolation, it has been confirmed in both of these species that increased mating time significantly correlates with increased mating success. Therefore, this might suggest that prey-gifts exploit female foraging motivation by attracting females and increasing their food supply. The initial attraction could be based on an exploitation of female foraging related sensory systems. Since females allow males to copulate with them while they are consuming the gift, male conspecifics that incorporate this courtship behavior might gain fitness benefits. This study also rules out the hypothesis that male Cladyenis, lost this gift-giving behavior while females retained it and thus, it did not descend from a gift-giving ancestor. The researchers confirmed this based on data from males of more recent genera who still exhibit this behavior. Based on molecular markers and previous phylogenies, genus Cladyenis branched off early in the Pisaura clade, which suggests that female preference for prey-carrying males most likely existed before the behavior did.

This study presents an interesting example of sensory exploitation. At the surface level, it does not seem that nuptial gift giving should exploit the female sensory system, as this behavior does not take the form of a signal directly. However, the receiver may still use cues and signals from the distressed or dead prey to make decisions and reduce mate choice uncertainty. In this case, the female may detect the gift even before the male, or detection of the male will increase with the addition of foraging cues. Furthermore, it might convey to the female that this is a strong mate who can forage and provide for young, which will allow females to discriminate between good quality and bad quality individuals. However, male spiders are often eaten after copulation or simply do not participate in food provisioning so this is most likely not the case. Since only certain species exhibit this behavior, it may function for species recognition but females in the present study still mated with heterospecifics. Since nuptial gift giving does not necessarily convey information about male quality and species recognition is not supported, the sensory exploitation hypothesis is reinforced. Future studies that attempt to investigate what is happening at a cognitive level during this behavior might reveal pertinent information regarding its exact function in courtship and sexual preference.


This entry was posted in What's New in Sensory Ecology?. Bookmark the permalink.

Leave a Reply