The role of silk threads as lifelines for caterpillars: pattern and significance of lifeline-climbing behaviour SHINJI SUGIURA 1 , 2 and KAZUO YAMAZAKI 3 1Graduate School of Human and Environmental Studies, Kyoto University, Japan, 2Department of Forest Entomology, Forestry and Forest Products Research Institute (FFPRI), Tsukuba, Japan and 3Osaka City Institute of Public Health and Environmental Sciences, Japan Abstract. 1. Most lepidopteran larvae use all of their legs (thoracic legs and abdominal prolegs) when walking on solid substrates. When caterpillars involun- tarily or intentionally drop from the tree canopy, they can regain their original position by climbing silk lifelines spun out from the head spinnerets. However, the taxonomic distribution of this climbing behaviour in the Lepidoptera is unknown. 2. Here, lifeline-climbing behaviour is reported in 13 lepidopteran species belonging to different taxa (five superfamilies and six families: Zygaenidae, Drepanidae, Geometridae, Lymantriidae, Noctuidae, and Nymphalidae). Caterpillars usually used only the three pairs of thoracic legs to climb lifelines, although they use different methods to walk on solid substrates, according to their taxonomic grouping and number of prolegs. 3. Results suggest that lifeline-climbing behaviour using only the thoracic legs is common among various lepidopteran taxa. The majority of species (12 of 13) climbed lifelines by alternating movement of the left and right set of thoracic legs, aided by side-to-side body movements. Only one of the 13 species, the geometrid Naxa seriaria (Motschulsky), climbed lifelines by drawing them down with its thoracic legs, aided by abdominal looping movements. While side-to-side move- ment of the abdomen was previously reported in lifeline climbing, this is the first report of the use of looping movements. Key words. Abdominal prolegs, antipredator defence, Geometridae, larvae, moths, thoracic legs. Introduction Lepidopteran larvae, or caterpillars, are major herbivores in forest canopies (Feeny, 1970). Caterpillars use silk threads spun out from the head spinnerets for various purposes (Craig, 1997), such as making nests (Fitzgerald, 1995), rolling and tying leaves (e.g. Fitzgerald et al., 1991 Fitzgerald & Clark, 1994), dispersing among and migrating from tree crowns (e.g. Elkinton & Liebhold, 1990 Murakami & Wada, 1997 Bell et al., 2005), capturing prey (Rubinoff & Haines, 2005), and building cocoons (e.g. Stehr, 1987). When disturbed or alarmed, some cater- pillars drop toward the ground and become suspended from the tree canopy by a silk lifeline spun out from the head spinnerets (Brackenbury, 1996 Oliveira & Freitas, 2004). How do these caterpillars return to the tree canopy? Brackenbury (1996) found that larvae of two microlepido- pteran species regained their original position by climbing back up the silk lines in two different ways. The first method was to use alternate movements of the left and right set of the thoracic legs, aided by side-to-side body movements (side-to-side movement type), while the second method involved the normal peristaltic rhythm that is used when walking on solid substrates (peristaltic rhythm type). These caterpillar behaviours have been observed under laboratory conditions and have been discussed in terms of kinematics (Brackenbury, 1996). However, these behaviours and their ecological significance have not been examined under field conditions. Furthermore, it is unclear Correspondence: S. Sugiura, Department of Forest Entomology, Forestry and Forest Products Research Institute (FFPRI), 1 Matsunosato, Tsukuba, Ibaraki 305-8687, Japan. E-mail: ssugiura@ ffpri.affrc.go.jp Ecological Entomology (2006) 31, 52���57 52 # 2006 The Authors Journal compilation # 2006 The Royal Entomological Society

whether these climbing behaviours are widespread among various lepidopteran lineages. Here, lifeline-climbing beha- viour is reported in 13 lepidopteran species, each belonging to a different taxon, under field conditions. Results suggest that lifeline-climbing behaviour is widespread among the Lepidoptera. Materials and method Morphological terminology and walking patterns of caterpillars Ninety-five per cent of all species of Lepidoptera belong to the Ditrysia, and their larvae are referred to as caterpil- lars. Caterpillars generally have three pairs of thoracic legs (true legs T1, T2, and T3) and five pairs of abdominal prolegs (A3, A4, A5, A6, and A10 Fig. 1a Stehr, 1987). When walking on solid substrates, free-living caterpillars normally engage all true legs and prolegs and crawl forward using a peristaltic wave that sweeps up the body from posterior to anterior (Brackenbury, 1997). However, there are many exceptions to this type of movement. For exam- ple, geometrid larvae lack three pairs of prolegs (A3, A4, and A5 Fig. 1b), and drepanid larvae lack the pair of anal prolegs (A10). This reduction in the number of prolegs is thought to aid in camouflage and rapid movement in these groups (Stehr, 1987 Weiss & Murphy, 1988). Unlike other larvae, when walking on solid substrates, geometrid larvae usually move in a characteristic looping manner by bring- ing the prolegs forward to rest close behind the thoracic legs, and then raising the anterior part of the body to locate a new footing (Stehr, 1987 Fig. 1b). Therefore, the num- bers of abdominal prolegs and walking styles differ among lepidopteran taxa. Methods The lifeline-climbing behaviour of caterpillars was exam- ined in six temperate deciduous forests in the Kinki region (34 170 35 090N, 135 090 135 470E, & 100���840 m above sea level), central Japan, from May to July 2004. When caterpillars were found suspended from tree crowns, their behaviour was observed. Most suspended caterpillars were motionless. For caterpillars observed climbing threads, the type of climbing behaviour and climbing speed under natural conditions were recorded. Climbing behaviour types were recorded as (I) side-to-side movement, (II) peri- staltic rhythm, or (III) other (according to Brackenbury, 1996). The climbing velocity of several species was also recorded by measuring the time (per 1.0 s) taken to travel 100 mm. Caterpillars were identified to species level on the basis of larval morphology using a colour catalogue (Sugi, 1987). Although climbing behaviours of all caterpillar species were observed under natural conditions, a novel behaviour in the geometrid Naxa seriaria (Motschulsky) was observed under conditions of artificial disturbance. After beating twigs, the behaviour of 11 N. seriaria larvae that dropped from the canopy was observed. Only Naxa seriaria lifeline-climbing behaviour was recorded using the movie function of a digital camera (Coolpix 995, Nikon, Tokyo, Japan) at 10 frames per second. Results and discussion The lifeline-climbing behaviour of 13 lepidopteran species was observed (Table 1). All observed caterpillars, which were middle to late instars, ascended the lifelines (silk threads) using only their thoracic legs (Table 1 Fig. 2a���c). Twelve species (92.3%) climbed by alternating movement of the left and right set of thoracic legs, without using the prolegs (Table 1 Fig. 3). Caterpillars bound the third set of thoracic legs (T3) with the threads, making balls of silk (Figs 2a,b and 3). The thread balls were not consumed by the caterpillars after their use, although the lifeline threads may represent a significant energetic investment. This type of climbing behaviour was identical to the side-to-side movement reported by Brackenbury (1996). This suggests that lifeline-climbing behaviour is common among various lepidopteran taxa (at least for eight families contained within seven superfamilies), despite differences in their walking styles and numbers of prolegs (Table 1). However, larvae of the geometrid Naxa seriaria (Motschulsky) climbed the lifelines using a different Head Thorax Abdomen Thoracic legs T1 T2 T3 T1 T2 T3 A3 A4 A5 A6 A6 A10 A10 Abdominal prolegs (Anal prolegs) Leg name Leg name (a) (b) Fig. 1. Caterpillar morphology. (a) Typical larval morphology and (b) larval morphology and walking method in the Geometridae. Arrows indicate the direction of movement. Silk threads as lifelines for caterpillars 53 # 2006 The Authors Journal compilation # 2006 The Royal Entomological Society, Ecological Entomology, 31, 52���57