Our data indicate that, in contrast to the previously accepted view, long-distance dispersal of the spiders in our study is not limited by selection to avoid encounters with water because individuals display behavioural adaptations that allow them to survive encounters with aquatic environments. The sailing-related behaviours that we observe are specific responses to landing on water because individuals do not show this behaviour when experiencing similar conditions in the absence of water. Furthermore, ballooning and sailing-related behaviours appear linked such that individuals that balloon are the most eager ‘sailors’.

Sailing appears to be found in almost all of the individuals that aerially disperse but the reverse is not true (Fig. 3). Sailing behaviour in non-ballooning spiders is likely to increase survival near the wet areas and might also be useful to survive after rainfall, including flooding events. By releasing silk on water, sailing spiders seem to act like ships dropping their anchors to slow down or stop their movement. Our observations suggest that a possibility could be that the silk may sometimes work as a dragline for the water-trapped spider to attach to floating objects or to the shore. A spider that reaches a floating tree, for example, might be able to become airborne by ballooning from its surface, or from one of its non-submerged branches. The possibility of taking off directly from the water’s surface seems unlikely as, when exposed to wind currents on water, rather than flying, spiders appeared to ‘slide’ across the surface. In fact, none of our experimental spiders showed the typical pre-ballooning tiptoeing behaviour on water.

Our data indicate that ballooning is either a polymorphic or a polyphenic behaviour, since not all the individuals belonging to the ballooning species tested here showed the intention to balloon. Interestingly our study also points towards the occurrence of local adaptation since the individuals used in our study, which were taken from small islands within a nature reserve, showed less overall propensity to balloon than individuals taken from wider habitats, such as farm lands, where ballooning capabilities have been previously tested using similar experimental conditions and methods [14]. Given that we have demonstrated the potential for genetic connectivity amongst populations even when separated by water, these results imply that this localised selection is strong enough to counteract the effects of gene flow from adjacent populations.

Ballooning tendency is known to be population-dependent even in extreme aeronautic spider species [36–39]. Several environmental factors are known to influence spiders’ propensity to balloon, including thermal conditions during juvenile stages [37], the level of disturbance of the habitat [38], food availability to parents and their life stage [39]. Other factors, such as the size of the habitat patches and isolation level, are consistent with an underlying genetic basis for the observed variation amongst populations [36]. The isolation level may be particularly relevant to the current study given that spiders were collected from islands of less than 0.16 ha. Local adaptations that decrease windborne dispersal in small habitats, such as these islands, once expected by Darwin, are frequently reported in other species.

The linyphiids and single tetragnathid spider species used in this work are small bodied and do balloon as adults. Others, such as Nephila pilipes (Araneae: Nephilidae), are large bodied and known to balloon only as tiny spiderlings [40]. It is possible, therefore, that our results are not that far reaching and may apply to only small spiders. However, our bibliographical searches and calculations show that most ballooning spiders collecting by trapping in the wild [25, 26, 31] have water repellent legs [41]. Thus, a phenotype predicted to confer water tolerance is associated with ballooning in the vast majority of species characterized so far from at least 4 different regions (East China 99 %, n = 104; USA 86 %, n = 1,982; Switzerland 94 %, n = 4,268 and Australia >99 %, n = 503). The association between this phenotype and ballooning tendency is consistent with physiological adaptations resulting in water tolerance being an underlying requirement for the adoption and maintenance of the airborne LDD strategy (Fig. 3). This, together with the fact that all the spiders studied here had water repelling legs, might point to a widespread occurrence of water tolerance and ability of spider species to move across the water’s surface. Trichobothria, which are sensory hairs on the spiders’ legs, might play a part in sensing wind and water currents, but given that they are found in species where no ‘sailing’ behaviour was observed, their function seems unlikely to be solely related to the persistence of these behavioural strategies. The almost complete association between ballooning and sailing, seen in Figs. 2 and 3, might even suggest that sailing behaviour might probably even be a requirement of aeronautic behaviour. Whatever the case, it is interesting to note how a small movement from a tiny spider’s leg could allow better survival on water and might potentially have far reaching evolutionary and ecosystem-wide impacts because ballooning behaviour is widespread and prevalent within this ecologically important group of predatory arthropods.