Eco-mechanics of lamellar autotomy in larval damselflies

Abstract

In larval damselflies, the self-amputation (autotomy) of the caudal lamellae permits escape from predatory larval dragonflies. Lamellar joint size declines among populations with increasing risk of dragonfly predation, but the breaking force required for autotomy and the biomechanical factors that influence breaking force are unknown. If autotomy enhances survival in larval damselflies, then predation by larval dragonflies should select for joints that require less force to break. We test this adaptive hypothesis by evaluating whether breaking force is negatively related to local predation risk from larval dragonflies. We also test a cuticle structure hypothesis, which predicts that breaking force is positively related to joint size and to joint cuticle thickness because of a structural support relationship between joint and lamella. The peak force necessary for lamellar autotomy was assessed on individual larval Enallagma damselflies collected from populations that varied in risk of predation. Easier lamellar autotomy occurred in larvae from sites with higher predation risk because damselflies from fishless ponds (where predatory larval dragonflies are likely more abundant) had lower breaking forces than those from ponds with fish (where larval dragonfly predation is likely reduced). Furthermore, breaking force was a positive function of joint size and also of total cuticle cross-sectional area after controlling for joint size. This suggests that autotomy may evolve in larval damselflies under selection from small grasping predators such as larval dragonflies by favouring smaller joint size or reduced cuticle area of lamellar joints.

Integrating trait multidimensionality, predation and autotomy to explain the maintenance of boldness

“…However, when the response was weak, larvae that (almost) never swam away had a higher probability of autotomy. Assuming a conscious component in lamellae autotomy in damselfly larvae (Gleason et al, 2014), this indicates that bold larvae compensated for their increased risk-taking behaviour in the presence of a predator with a higher probability of autotomy, consistent with a scenario of trait compensation (DeWitt et al, 1999). This is partly in accordance with the study of Kuo et al (2015) where bold lizards autotomised their tail more readily.…”

“…While autotomy involves a reflex process, the propensity for autotomy is also believed to be under conscious control in several taxa (e.g. Kuo et al, 2015), including damselfly larvae (Gleason, Fudge, & Robinson, 2014). The combination of swimming propensity and response to predator cues determined the probability of autotomy (similar to correlational selection).…”

The ecology and evolution of autotomy

“…Thus, this hypothesis can be considered one of morphological and physiological constraints. Previous studies have investigated the amount of force it takes to break an autotomy fracture plane in both vertebrates [lizards (Fox, Perea‐Fox, & Franco, ; Fox, Conder, & Smith, )] and invertebrates [damselflies (Gleason, Fudge, & Robinson, ), starfish (Marrs et al, ), crabs (Prestholdt et al, )]. However, these studies often fail to identify the amount of time it takes an organism to generate the same amount of force and assume that the amount of force required to perform autotomy positively correlates with the latency to autotomize.…”

Integrative biology of injury in animals

“…Selection may even act on diverging strategies within the same structure or trait. For example, studies in damselfly larvae indicate a link between lamellar joint allometry and environmental predation risk, where smaller, weaker joints are correlated with increasing predation risk (Gleason, Fudge & Robinson, 2014 ), presumably reflecting past and ongoing selection to facilitate autotomy or breakage by direct predation, whereas larger, stronger joints enhance swimming in low‐predation risk environments (Bose & Robinson, 2013 ). Injury‐related phenomena that have evolved repeatedly across animals, such as autotomy and changes in regenerative ability, provide particularly powerful frameworks for disentangling the many factors that shape the evolution of injury responses.…”