Testing presence of directionality information in female spider silk trails through male trail-following behavior

Mate search is challenging for solitary species. Trails represent a particularly potent, target-oriented means for finding mates, as trail-following increases encounter rates between individuals compared to random search. Embedding directionality information into the trail allows individuals to follow trails correctly to the source. Yet, directionality remains poorly understood. Spiders deposit trails during locomotion consisting of silk lines and substrate-borne chemicals. We conducted multiple experiments to test whether female silk trails convey directionality information, whether directionality is chemically or structurally encoded and depends on female phenotype. We also examined whether males interact with silk in a way that suggests information gathering. We exposed males of the cursorial spider Pisaura mirabilis to female trails deposited unidirectionally and scored their trail-following direction (i.e., same as or opposite to the females'). Tests were repeated after washing trails with a solvent to remove putative chemicals and by sourcing silk from females of different feeding regimes. While we found little evidence for male directional trail-following, we did find that unwashed trails were more likely to be followed than washed trails. Similarly, trails of relatively larger females were more likely to be followed correctly than those of smaller females. Males extensively probed and pulled on silk lines with their appendages, suggesting the gathering of chemical and tactile information. Taken together, results suggest that directional trail-following is selected only under specific contexts in this species. Chemical attributes of trails may convey information on female quality, with directional trail-following reflecting male mate choice in a system characterized by costly male nuptial gifts. Significance statement In the context of male mate search, following conspecific trails increases the chances of encountering a mating partner, especially if trails provide information about the direction the conspecific went. Yet, trail directionality remains poorly understood. Female spiders deposit silk trails as they walk. We overall show that males follow trails directionally only under a specific context. Males were more likely to follow correctly when trails were unmanipulated (compared to being washed with solvents to remove chemicals) and when they were deposited by relatively larger females (compared to smaller ones). Chemical attributes of trails may potentially indicate directionality, while decoding movement direction from trails of larger females may reflect male preferences for females of higher reproductive value.