A novel power-amplified jumping behavior in larval beetles (Coleoptera: Laemophloeidae).

Matthew A Bertone,Ainsley E Seago,Takahiro Yoshida,Adrian A Smith,Joshua C Gibson,Phillip Barden

doi:10.1371/journal.pone.0256509

Abstract

Larval insects use many methods for locomotion. Here we describe a previously unknown jumping behavior in a group of beetle larvae (Coleoptera: Laemophloeidae). We analyze and describe this behavior in Laemophloeus biguttatus and provide information on similar observations for another laemophloeid species, Placonotus testaceus. Laemophloeus biguttatus larvae precede jumps by arching their body while gripping the substrate with their legs over a period of 0.22 ± 0.17s. This is followed by a rapid ventral curling of the body after the larvae releases its grip that launches them into the air. Larvae reached takeoff velocities of 0.47 ± 0.15 m s-1 and traveled 11.2 ± 2.8 mm (1.98 ± 0.8 body lengths) horizontally and 7.9 ± 4.3 mm (1.5 ± 0.9 body lengths) vertically during their jumps. Conservative estimates of power output revealed that some but not all jumps can be explained by direct muscle power alone, suggesting Laemophloeus biguttatus may use a latch-mediated spring actuation mechanism (LaMSA) in which interaction between the larvae's legs and the substrate serves as the latch. MicroCT scans and SEM imaging of larvae did not reveal any notable modifications that would aid in jumping. Although more in-depth experiments could not be performed to test hypotheses on the function of these jumps, we posit that this behavior is used for rapid locomotion which is energetically more efficient than crawling the same distance to disperse from their ephemeral habitat. We also summarize and discuss jumping behaviors among insect larvae for additional context of this behavior in laemophloeid beetles.

Highlights

The larvae collected in North Carolina, USA (Fig 3A) were initially identified morphologically as Laemophloeidae based on their anatomy and the abundance of adults (Laemophloeus biguttatus (Say); Fig 3B) associated with the fungus
The results of our power density calculations for jumps provide a reasonable case for direct muscle action alone being insufficient to explain jump power for these larvae
The majority of jumps fall beneath our established 400 W/kg cutoff point for power amplification in all scenarios examined, this cutoff point is based on measurements from muscles that have been naturally selected for extraordinarily high sustained power output, and it is unlikely that actual power output of the larvae’s muscles are that high

Summary

Introduction

The extraordinary evolutionary success of holometabolous insects can be partially attributed to their partitioned life history: immatures (larvae) are often soft-bodied and minimally. Exceptions include a few groups containing active predators (e.g. Carabidae and Chrysopidae) and triungulin or planidial larvae, in which the highly mobile first instar locates a host before reverting to a largely immobile, parasitic form in subsequent instars (referred to as hypermetamorphosis) [4] Despite these limitations, several insect lineages have evolved distinctive methods of rapid larval locomotion without using legs at all. Ceratitis larvae achieve jumps of up to 150 times their body length by curling into a loop and pumping hemolymph into the abdominal segments until the resulting turgor pressure is sufficient for bodily propulsion when the loop is released [28] This body loop is anchored by attachment of the mandibles to the sclerotized anal plate, effectively forming a latch-mediated spring [46]. We report observations of a similar behavior in another laemophloeid beetle larva, Placonotus testaceus (F.), and present a brief review of jumping behaviors in insect larvae

Materials and methods

Results

Discussion