Reproductive biology of harvestmen (Arachnida: Opiliones): a review of a rapidly evolving research field

Abstract

Harvestmen are a major arachnid order that has experienced a dramatic increase in biological knowledge in the 21 st century. The publication of the book Harvestmen: The Biology of Opiliones in 2007 stimulated development of many behavioral studies. Although the book is relatively recent, our understanding of the reproductive biology of harvestmen is already outdated due to the fast accumulation of new data. Our goal is to provide an updated review of the subject to serve as benchmark for the following years. In the pre-copulatory phase, we explore the evolution of facultative parthenogenesis, the factors that may affect the types of mating system, and the role of nuptial gifts in courtship. Regarding the copulatory phase, harvestmen are unique arachnids because they have aflagellate spermatozoa and a penis with complex morphology. We discuss the implications of these two features for sperm competition and cryptic female choice. In the post-copulatory phase, we connect oviposition site selection and climate conditions to the widespread occurrence of resource defense polygyny, alternative reproductive tactics, and sexual dimorphism in several clades of tropical harvestmen. Finally, we present the different forms of parental care in the order, and discuss the benefits and costs of this behavior, which can be performed either by females or males. Throughout the review, we indicate gaps in our knowledge and subjects that deserve further studies. Hopefully, the information synthesized here will stimulate researchers worldwide to embrace harvestmen as a study system and to improve our effort to unravel the mysteries of their reproductive biology.

The reduction of nuptial gifts in sclerosomatid Opiliones coincides with increased behavioural sexual conflict

“…Burns and Shultz (2016) additionally cite reports of males with broken penises in the field, an injury consistent with struggles to disengage females. Evidence from crickets and spiders supports the notion that female aggression can negatively correlate with nuptial gift quality and quantity (Kuriwada & Kasuya 2012; Toft & Albo 2016), and in L. vittatum this manipulation by females might be the direct result of the deterioration of nuptial gift quality and the loss of a precopulatory nuptial gift (Khan et al 2018; Machado & Burns 2023; Machado & Macías-Ordόñez 2007). Because females of nonsacculate species can only receive nuptial gift fluid during intromission, rather than both before and during, there may be a tangible benefit to females remaining in copula as long as possible.…”

“…Burns and colleagues have described repeated correlated evolution of both female and male reproductive morphology, revealing two primary reproductive syndromes (Burns et al 2012(Burns et al , 2013: 1) An ancestral, sacculate state in which males have terminal nuptial gift sacs on their penises and females do not have pregenital barriers; and 2) a derived, nonsacculate state in which males do not have terminal nuptial gift sacs on their penises and females have pregenital barriers. Both sacculate and nonsacculate Leiobunum harvesters produce nuptial gifts to some degree, although the presence of terminal nuptial gift sacs increases the quantity transferred to females during mating interactions and allows for precopulatory transfer (Machado & Burns 2023;Machado & Macías-Ordóñez 2007). Sacculate females receive nuptial gift fluid before and during copulation, while nonsacculate females can only receive it during copulation (Figure 1).…”

“…Nonsacculate species tend to have more robust genital biomechanics, specialised clasping structures, and less nutritious nuptial gifts, while sacculate species tend to have less robust genital biomechanics, unspecialized clasping structures, and higher-value nuptial gifts (Burns et al 2013;Burns & Shultz 2015Kahn et al 2018;Machado & Burns 2023). Although there is morphological and chemical evidence of a shift towards increased conflict, comparative behavioural evidence in the genus is limited.…”

“…Sacculate females receive nuptial gift fluid before and during copulation, while nonsacculate females can only receive it during copulation (Figure 1). In addition to these genital morphologies, sacculate and nonsacculate species also differ in genital biomechanics (Burns & Shultz 2015, 2016), somatic morphology (Burns et al 2013; Machado & Burns 2023), and nuptial gift biochemistry (Kahn et al 2018). Nonsacculate species tend to have more robust genital biomechanics, specialised clasping structures, and less nutritious nuptial gifts, while sacculate species tend to have less robust genital biomechanics, unspecialized clasping structures, and higher-value nuptial gifts (Burns et al 2013; Burns & Shultz 2015, 2016; Kahn et al 2018; Machado & Burns 2023).…”

Coverings on Pitfall Traps Influence the Abundance of Ground-Dwelling Arthropods

“…However, traps without covers tended to attract a generally larger number of harvestmen species, although not significantly more than translucent covers. Unlike juveniles, adult harvestmen may spend a significant proportion of their time searching for mates in vegetation [49]. Therefore, the sexual activity of adults may explain differences in capture rates between juveniles and adults.…”