Why caterpillars do not grow short and fat

doi:10.1016/0020-7322(93)90002-I

International Journal of Insect Morphology and Embryology

Volume 22, Issues 2–4, April–October 1993, Pages 81-102

International Journa...

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Abstract

The integument of a caterpillar consists of a cuticle that is structurally isotropic in the plane of the surface, overlaying an epidermis and basal lamina. Between ecdyses the cuticle stretches so that the proportions of caterpillars are about the same at the end of a stadium as at the beginning. This introduces a paradox, since under uniform internal hydrostatic pressure, the hoop stress is twice the axial stress. Stress in the integument of a caterpillar inflated by compressed hemolymph would be twice as great in the circumference as in the axis, causing it to become progressively fatter in proportion to its length as it grows. This does not happen because axial pleats allow caterpillar cuticle to extend more easily in the axis, allowing uniform growth in spite of the greater hoop stress from internal hydrostatic pressure.

References (20)

W.V. Condoulis et al.
The deposition of endocuticle in insects
J. Insect Physiol.
(1966)
H.R. Hepburn
Structure of the integument
A.C. Kotze et al.
Mechanical properties of the cuticle of Manduca sexta larvae treated with cyromazine
Pestic. Biochem. Physiol.
(1990)
M. Locke
The moult/intermoult cycle in the epidermis and other tissues of an insect Calpodes ethlius (Lepidoptera, Hesperiidae)
Tissue Cell
(1970)
M. Locke
The structure of epidermal feet during their development
Tissue Cell
(1985)
M. Locke
The very rapid induction of filopodia in insect cells
Tissue Cell
(1987)
M. Locke et al.
Epidermal feet in pupal segment morphogenesis
Tissue Cell
(1981)
P. Delhanty et al.
The development of epidermal feet in preparation for metamorphosis in an insect
Tissue Cell
(1990)
J.E. Gordon
Structures, or Why Things Don't Fall Down
(1978)
P.B. Hughes et al.
Inhibition of growth and development of tobacco hornworm (Lepidoptera : Sphingidae) larvae by Cyromazine
J. Econ. Entomol.
(1989)

There are more references available in the full text version of this article.

Cited by (13)

Localization of RR-1 and RR-2 cuticular proteins within the cuticle of Anopheles gambiae
2017, Arthropod Structure and Development
Citation Excerpt :
Thus, they concluded: “From the present results, RR-2 CP appears to be involved in the exocuticle and RR-1 in exo- and endocuticle layers.” A complication of using transcript appearance to predict protein localization is the evidence that newly secreted CPs can be interspersed in older regions of the cuticle, a phenomenon called intussusception (Carter and Locke, 1993). Obviously transcript data are only a very indirect way of assessing the location of CPR proteins.
The largest arthropod cuticular protein family, CPR, has the Rebers and Riddiford (R&R) Consensus that in an extended form confers chitin-binding properties. Two forms of the Consensus, RR-1 and RR-2, have been recognized and initial data suggested that the RR-1 and RR-2 proteins were present in different regions within the cuticle itself. Thus, RR-2 proteins would contribute to exocuticle that becomes sclerotized, while RR-1s would be found in endocuticle that remains soft. An alternative, and more common, suggestion is that RR-1 proteins are used for soft, flexible cuticles such as intersegmental membranes, while RR-2s are associated with hard cuticle such as sclerites and head capsules. We used TEM immunogold detection to localize the position of several RR-1 and RR-2 proteins in the cuticle of Anopheles gambiae. RR-1s were localized in the procuticle of the soft intersegmental membrane except for one protein found in the endocuticle of hard cuticle. RR-2s were consistently found in hard cuticle and not in flexible cuticle. All RR-2 antibodies localized to the exocuticle and four out of six were also found in the endocuticle. Hence the location of RR-1s and RR-2s depends more on properties of individual proteins than on either hypothesis.
Cuticular Proteins
2012, Insect Molecular Biology and Biochemistry
This chapter summarizes the wealth of information about cuticular proteins amassed. Cuticular protein sequences are certain to be described in ever-increasing numbers as more insect genomes are analyzed. Central to the issue of cuticle structure is the important fact that considerable cuticle growth can occur during an intermolt period, some of it by a smoothing out of macro- and microscopic folds and pleats. During intra-instar growth, new cuticular proteins are interspersed among the old, necessitating a model of chitin–protein and protein–protein interactions that will permit such intussusception. A wealth of sequence information is available for cuticular proteins, but many challenges lie ahead for those who wish to continue to further their understanding of how the diverse forms and properties of cuticle are constructed extracellularly as these proteins self-assemble in proximity to chitin and make specific contributions to the properties of the exoskeleton.
Cuticular Proteins
2011, Insect Molecular Biology and Biochemistry
This chapter summarizes the wealth of information about cuticular proteins amassed. Cuticular protein sequences are certain to be described in ever-increasing numbers as more insect genomes are analyzed. Central to the issue of cuticle structure is the important fact that considerable cuticle growth can occur during an intermolt period, some of it by a smoothing out of macro- and microscopic folds and pleats. During intra-instar growth, new cuticular proteins are interspersed among the old, necessitating a model of chitin–protein and protein–protein interactions that will permit such intussusception. A wealth of sequence information is available for cuticular proteins, but many challenges lie ahead for those who wish to continue to further their understanding of how the diverse forms and properties of cuticle are constructed extracellularly as these proteins self-assemble in proximity to chitin and make specific contributions to the properties of the exoskeleton.
Visceral-locomotory pistoning in crawling caterpillars
2010, Current Biology
Citation Excerpt :
The gut can be described as a cylindrical, nonlinear elastic mass that extends from the terminal segment to the head. The caterpillar body wall and musculature constitute a soft shell around the gut, the cuticle resembling a woven tube [19, 20] and the musculature resembling a complicated, repeating series of primarily longitudinal and oblique muscles [21–23]. Within the crawling caterpillar's body wall, the gut shortens and slides forward during the terminal proleg swing phase, resulting in a shift forward of the animal's center of mass (CoM).
Animals with an open coelom do not fully constrain internal tissues [1, 2, 3], and changes in tissue or organ position during body movements cannot be readily discerned from outside of the body. This complicates modeling of soft-bodied locomotion, because it obscures potentially important changes in the center of mass as a result of internal tissue movements [4, 5]. We used phase-contrast synchrotron X-ray imaging [6, 7, 8, 9, 10] and transmission light microscopy to directly visualize internal soft-tissue movements in freely crawling caterpillars. Here we report a novel visceral-locomotory piston in crawling Manduca sexta larvae, in which the gut slides forward in advance of surrounding tissues. The initiation of gut sliding is synchronous with the start of the terminal prolegs' swing phase, suggesting that the animal's center of mass advances forward during the midabdominal prolegs' stance phase and is therefore decoupled from visible translations of the body. Based on synchrotron X-ray data and transmission light microscopy results, we present evidence for a two-body mechanical system with a nonlinear elastic gut that changes size and translates between the anterior and posterior of the animal. The proposed two-body system—the container and the contained—is unlike any form of legged locomotion previously reported and represents a new feature in our emerging understanding of crawling.
Soft-cuticle biomechanics: A constitutive model of anisotropy for caterpillar integument
2009, Journal of Theoretical Biology
Citation Excerpt :
Early work by Carter and Locke directly addressed this paradox. Using microscopic and histological techniques, they showed how during growth soft cuticle expands more in the axial than the circumferential direction through the unfolding of microscopic pleats in the endocuticle (Carter and Locke, 1993). While stretching causes reinforcing fiber realignment in the circumferential direction, the axial pleats reduce this realignment along the animal's axis.
The mechanical properties of soft tissues are important for the control of motion in many invertebrates. Pressurized cylindrical animals such as worms have circumferential reinforcement of the body wall; however, no experimental characterization of comparable anisotropy has been reported for climbing larvae such as caterpillars. Using uniaxial, real-time fluorescence extensometry on millimeter scale cuticle specimens we have quantified differences in the mechanical properties of cuticle to circumferentially and longitudinally applied forces. Based on these results and the composite matrix–fiber structure of cuticle, a pseudo-elastic transversely isotropic constitutive material model was constructed with circumferential reinforcement realized as a Horgan–Saccomandi strain energy function. This model was then used numerically to describe the anisotropic material properties of Manduca cuticle. The constitutive material model will be used in a detailed finite-element analysis to improve our understanding of the mechanics of caterpillar crawling.
Cuticular Proteins
2005, Comprehensive Molecular Insect Science

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International Journal of Insect Morphology and Embryology

Abstract

References (20)

The deposition of endocuticle in insects

J. Insect Physiol.

Structure of the integument

Mechanical properties of the cuticle of Manduca sexta larvae treated with cyromazine

Pestic. Biochem. Physiol.

The moult/intermoult cycle in the epidermis and other tissues of an insect Calpodes ethlius (Lepidoptera, Hesperiidae)

Tissue Cell

The structure of epidermal feet during their development

Tissue Cell

The very rapid induction of filopodia in insect cells

Tissue Cell

Epidermal feet in pupal segment morphogenesis

Tissue Cell

The development of epidermal feet in preparation for metamorphosis in an insect

Tissue Cell

Structures, or Why Things Don't Fall Down

Inhibition of growth and development of tobacco hornworm (Lepidoptera : Sphingidae) larvae by Cyromazine

J. Econ. Entomol.

Cited by (13)

Localization of RR-1 and RR-2 cuticular proteins within the cuticle of Anopheles gambiae

Cuticular Proteins

Cuticular Proteins

Visceral-locomotory pistoning in crawling caterpillars

Soft-cuticle biomechanics: A constitutive model of anisotropy for caterpillar integument

Cuticular Proteins