Abstract
The late 5th instar caterpillar of the cecropia silk moth (Hyalophora cecropia) spins a silken cocoon with a distinct, multilayered architecture. The cocoon construction program, first described by the seminal work of Van der Kloot and Williams, consists of a highly ordered sequence of events. We perform behavioral experiments to re-evaluate the original cecropia work, which hypothesized that the length of silk that passes through the spinneret controls the orderly execution of each of the discrete events of cocoon spinning. We confirm and extend by three-dimensional scanning and quantitative measurements of silk weights that if cocoon construction is interrupted, upon re-spinning, the caterpillar continues the cocoon program from where it left off. We also confirm and extend by quantitative measurements of silk weights that cecropia caterpillars will not bypass any of the sections of the cocoon during the construction process, even if presented with a pre-spun section of a cocoon spun by another caterpillar. Blocking silk output inhibits caterpillars from performing normal spinning behaviors used for cocoon construction. Surprisingly, unblocking silk output 24-hr later did not restart the cocoon construction program, suggesting the involvement of a temporally-defined interval timer. We confirm with surgical reductions of the silk glands that it is the length of silk itself that matters, rather than the total amount of silk extracted by individuals. We used scanning electron microscopy to directly show that either mono- or dual-filament silk (i.e., equal silk lengths but which vary in their total amount of silk extracted) can be used to construct equivalent cocoons of normal size and that contain the relevant layers. We propose that our findings, taken together with the results of prior studies, strongly support the hypothesis that the caterpillar uses a silk “odometer” to measure the length of silk extracted during cocoon construction but does so in a temporally regulated manner. We further postulate that our examination of the anatomy of the silk spinning apparatus and ablating spinneret sensory output provides evidence that silk length measurement occurs upstream of output from the spinneret.
Highlights
Many animals have evolved with the ability to measure quantities
Interruption was attained by removing caterpillars (n = 8) that had already spun a clearly-delineated outer envelope (OE) encasing the caterpillar, designated an initial OE (Fig 2A, leftside of left panel); a distinct compact initial OE was formed between 15 and 21 hrs after the completed, impregnated OE at 32 hrs after the onset of cocoon construction and a longitudinal, sagittal section of the inner envelope (IE) spun on 2nd spin with attached fragments of the intermediate space (IS)
That the spinneret is important for the control of the length-coupled behavioral repertoire is reinforced by the finding that either mono- or dual-filament silk can be used to fully construct a cocoon containing both the OE and IE (Fig 7; ref 7)
Summary
The ability to perform such measurements is a key aspect of motor programs that guide ecologically relevant movement behavior in time and space [1]. Several arthropods such as desert ants [2,3], salticid spiders [4], and fiddler crabs [5] appear to possess odometer mechanisms that allow them to measure distance to perform accurate and precise homing behavior across a variety of landscapes [1]. In addition to measuring distance, i.e., a measurement of how far apart two objects or points are, such a biological odometer mechanism could function to measure the length of a three-dimensional (3D) object within one dimension, such as the length of self-generated materials like the silk fiber used for the construction of moth cocoons and spider webs. Constructed by late 5th instar larvae during the summer, cocoons serve as important overwintering housing for individuals during the pupal stage, and from which individuals will later eclose as adults in the following spring [10,11,12]
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