Ballooning dispersal using silk: world fauna, phylogenies, genetics and models

Abstract

Aerial dispersal using silk ('ballooning') has evolved in spiders (Araneae), spider mites (Acari) and in the larvae of moths (Lepidoptera). Since the 17th century, over 500 observations of ballooning behaviours have been published, yet there is an absence of any evolutionary synthesis of these data. In this paper the literature is reviewed, extensively documenting the known world fauna that balloon and the principal behaviours involved. This knowledge is then incorporated into the current evolutionary phylogenies to examine how ballooning might have arisen. Whilst it is possible that ballooning co-evolved with silk and emerged as early as the Devonian (410-355 mya), it is arguably more likely that ballooning evolved in parallel with deciduous trees, herbaceous annuals and grasses in the Cretaceous (135-65 mya). During this period, temporal (e.g. bud burst, chlorophyll thresholds) and spatial (e.g. herbivory, trampling) heterogeneities in habitat structuring predominated and intensified into the Cenozoic (65 mya to the present). It is hypothesized that from the ancestral launch mechanism known as 'suspended ballooning', widely used by individuals in plant canopies, 'tip-toe' and 'rearing' take-off behaviours were strongly selected for as habitats changed. It is contended that ballooning behaviour in all three orders can be described as a mixed Evolutionary Stable Strategy. This comprises individual bet-hedging due to habitat unpredictability, giving an underlying randomness to individual ballooning, with adjustments to the individual ballooning probability being conferred by more predictable habitat changes or colonization strategies. Finally, current methods used to study ballooning, including modelling and genetic research, are illustrated and an indication of future prospects given.

Geographical variation in wolf spider dispersal behaviour is related to landscape structure

“…Flight control also assumes the presence of sensory systems for environmental perception, but olfaction and vision are weakly developed even at small distances in actively hunting arthropod species with passive aerial dispersal ). Regardless of whether individuals are able to change velocity by adjusting postures (Suter 1992) or thread lengths (Bell et al 2005), the nature of the currents remains intrinsically unpredictable. As a consequence, the uncertainty of reaching suitable habitat remains high when individuals take the decision to disperse.…”

“…wings in aphids and waterstriders; Zera & Denno 1997) or behavioural dispersal properties (e.g. unique predispersal behaviour in spiders, mites and caterpillars; Bell et al 2005), morphological variation (e.g. in wing size) between populations probably does not reflect selection for dispersal, but rather relates to thermoregulation (Kemp & Krockenberger 2004), predator avoidance (Rydell & Lancaster 2000) or selection for other genetically correlated traits (Roff 1997;Mazer & Damuth 2001 …”

“…As in all species of wolf spiders, physical constraints restrict aerial dispersal during the first two (sometimes three) instars (Richter 1970;Bell et al 2005) and maternal effects may preadapt offspring to the ambient conditions they are likely to encounter in their natal habitat at later stages. We studied propensity for aerial dispersal under standardized laboratory conditions (i.e.…”

“…The prevalence of this behaviour is a good precursor of effective aerial dispersal (Weyman et al 1995;D. Bonte, unpublished data), although we cannot separate inter-and intrapopulation dispersal, as this is determined by wind velocity (Bell et al 2005). We studied variation in tiptoe behaviour among offspring originating from females collected in three areas of dunes differing in population structure (continuous, fragmented and isolated populations) and among four subpopulations of the fragmented population from the Flemish coast (Bonte et al 2003c).…”

“…Unlike winged arthropods, spiders (Araneae) and mites (Acaridae) often perform aerial dispersal in a predominantly uncontrolled mode (e.g. Weyman 1993;Weyman et al 2002), thereby entering suitable habitats largely by chance (Bell et al 2005). …”