The role of the foregut in digestion in the cricket Teleogryllus commodus and the locust Chortoicetes terminifera
ShangXian Zhou A , James D. Woodman B , Hua Chen C and Paul D. Cooper A DA Ecology and Evolution, Research School of Biology, The Australian National University, Canberra, ACT 2601, Australia.
B Australian Government Department of Agriculture, Water and the Environment, GPO Box 858, Canberra, ACT 2601, Australia.
C Centre for Advanced Microscopy, The Australian National University, Canberra, ACT 2601, Australia.
D Corresponding author. Email: paul.cooper@anu.edu.au
Australian Journal of Zoology 68(4) 212-221 https://doi.org/10.1071/ZO20092
Submitted: 13 November 2020 Accepted: 28 July 2021 Published: 26 August 2021
Abstract
The role of the foregut (crop and proventriculus) in mechanical processing of food has received little attention in insects. Using the Australian plague locust (Chortoicetes terminifera) and the black field cricket (Teleogryllus commodus) as models, the role of the crop in processing of wheat or rye grass was examined. Interior cuticular structures (spines) of the foregut were described using light and scanning electron microscopy, with locusts having sclerotised structures and crops of crickets being unsclerotised internally. Muscular bands on the exterior surface of the crop part of the foregut are similar in males of both species, but contractions and movements are more forceful in locusts. Passage rate from the foregut is much faster in locusts (<3 h) than in crickets (>3 h). Water within the crop is reduced compared with the water content of fresh grass within the foregut of locusts, but water is increased in cricket crops. Spines within the crops are small relative to the size of food particles in both species. Some spines of locusts contain metals. The slower passage rate from the crop of crickets may be limited by the proventriculus. Foregut structure and food processing facilitates the generalist diet of crickets, but may restrict locusts to consuming softer grasses.
Keywords: Orthoptera, physiology, morphology, digestion, passage rate, cuticular nanostructures.
References
Adriaansen, C., Woodman, J. D., Deveson, E., and Drake, V. A. (2016). The Australian plague locust – risk and response. In ‘Biological and Environmental Hazards, Risks, and Disasters’. (Ed. R. Sivanpillai.) pp. 67–86. (Elsevier: Oxford, UK.)Baines, D. M., Bernays, E. A., and Leather, E. M. (1973). Movement of food through the gut of fifth-instar males of Locusta migratoria migratorioides (R. & F.). Acrida 2, 319–332.
Baker, C. (2011). Cricket plague – should we be jumping for cover. Environment Institute Blog, University of Adelaide.
Bentos-Pereira, A., and Lorier, E. (1992). Cuticular structures of the stomodeum in Paulinia acuminata (De Geer) and Marellia remipes Uvarov (Orthoptera: Pauliniidae). International Journal of Insect Morphology & Embryology 21, 161–174.
| Cuticular structures of the stomodeum in Paulinia acuminata (De Geer) and Marellia remipes Uvarov (Orthoptera: Pauliniidae).Crossref | GoogleScholarGoogle Scholar |
Bernays, E. A., and Chapman, R. F. (1973). The role of food plants in the survival and development of Chortoicetes terminifera (Walker) under drought conditions. Australian Journal of Zoology 21, 575–592.
| The role of food plants in the survival and development of Chortoicetes terminifera (Walker) under drought conditions.Crossref | GoogleScholarGoogle Scholar |
Biagio, F. P., Tamaki, F. K., Terra, W. R., and Ribeiro, A. F. (2009). Digestive morphophysiology of Gryllodes sigillatus (Orthoptera: Gryllidae). Journal of Insect Physiology 55, 1125–1133.
| Digestive morphophysiology of Gryllodes sigillatus (Orthoptera: Gryllidae).Crossref | GoogleScholarGoogle Scholar | 19715697PubMed |
Blank, R. H., and Olson, M. H. (1981). The damage potential of the black field cricket Teleogryllus commodus. New Zealand Journal of Agricultural Research 24, 251–258.
| The damage potential of the black field cricket Teleogryllus commodus.Crossref | GoogleScholarGoogle Scholar |
Chapman, R. F. (1995). Mechanics of food handling by chewing insects. In ‘Regulatory Mechanisms in Insect Feeding’. (Eds R. F. Chapman, and G. de Boer.) pp. 3–31. (Chapman & Hall: New York.)
Cheeseman, M. T., and Pritchard, G. (1984). Proventricular trituration in adult carabid beetles (Coleoptera, Carabidae). Journal of Insect Physiology 30, 203–209.
| Proventricular trituration in adult carabid beetles (Coleoptera, Carabidae).Crossref | GoogleScholarGoogle Scholar |
Clissold, F. J. (2007). The biomechanics of chewing and plant fracture: mechanisms and implications. Advances in Insect Physiology: Insect Mechanics and Control 34, 317–372.
| The biomechanics of chewing and plant fracture: mechanisms and implications.Crossref | GoogleScholarGoogle Scholar |
Clissold, F. J., Sanson, G. D., and Read, J. (2006). The paradoxical effects of nutrient ratios and supply rates on an outbreaking insect herbivore, the Australian plague locust. Journal of Animal Ecology 75, 1000–1013.
| The paradoxical effects of nutrient ratios and supply rates on an outbreaking insect herbivore, the Australian plague locust.Crossref | GoogleScholarGoogle Scholar |
Cooper, P. D., and He, P. H. (1994). Control of foregut contraction in the black field cricket, Teleogryllus commodus Walker (Orthoptera, Gryllidae). Journal of Insect Physiology 40, 475–481.
| Control of foregut contraction in the black field cricket, Teleogryllus commodus Walker (Orthoptera, Gryllidae).Crossref | GoogleScholarGoogle Scholar |
Cooper, P. D., and Vulcano, R. (1997). Regulation of pH in the digestive system of the cricket, Teleogryllus commodus Walker. Journal of Insect Physiology 43, 495–499.
| Regulation of pH in the digestive system of the cricket, Teleogryllus commodus Walker.Crossref | GoogleScholarGoogle Scholar |
Cribb, B. W., Stewart, A., Huang, H., Truss, R., Noller, B., Rasch, R., and Zalucki, M. P. (2008). Insect mandibles – comparative mechanical properties and links with metal incorporation. Naturwissenschaften 95, 17–23.
| Insect mandibles – comparative mechanical properties and links with metal incorporation.Crossref | GoogleScholarGoogle Scholar | 17646951PubMed |
Elzinga, R. J. (1996). A comparative study of microspines in the alimentary canal of five families of Orthoptera (Saltatoria). International Journal of Insect Morphology & Embryology 25, 249–260.
| A comparative study of microspines in the alimentary canal of five families of Orthoptera (Saltatoria).Crossref | GoogleScholarGoogle Scholar |
Ferreira, C., Oliveira, M. C., and Terra, W. R. (1990). Compartmentalization of the digestive process in Abracris flavolineata (Orthoptera: Acrididae) adults. Insect Biochemistry 20, 267–274.
| Compartmentalization of the digestive process in Abracris flavolineata (Orthoptera: Acrididae) adults.Crossref | GoogleScholarGoogle Scholar |
Gangwere, S. (1966). The mechanical handling of food by the alimentary canal of Orthoptera and allies. EOS. Revista Española de Entomología 41, 247–265.
Hillerton, J. E., and Vincent, J. F. V. (1982). The specific location of zinc in insect mandibles. The Journal of Experimental Biology 101, 333–336.
| The specific location of zinc in insect mandibles.Crossref | GoogleScholarGoogle Scholar |
Hillerton, J. E., Robertson, B., and Vincent, J. F. V. (1984). The presence of zinc or manganese as the predominant metal in the mandibles of adult, stored-product beetles. Journal of Stored Products Research 20, 133–137.
| The presence of zinc or manganese as the predominant metal in the mandibles of adult, stored-product beetles.Crossref | GoogleScholarGoogle Scholar |
Hochuli, D. F., Roberts, B., and Sanson, G. D. (1992). Anteriorly directed microspines in the foregut of Locusta migratoria (Orthoptera: Acrididae). International Journal of Insect Morphology & Embryology 21, 95–97.
| Anteriorly directed microspines in the foregut of Locusta migratoria (Orthoptera: Acrididae).Crossref | GoogleScholarGoogle Scholar |
Hochuli, D. F., Roberts, B., and Sanson, G. D. (1994). Foregut morphology of Locusta migratoria (L) (Orthoptera, Acrididae). Journal of the Australian Entomological Society 33, 65–69.
| Foregut morphology of Locusta migratoria (L) (Orthoptera, Acrididae).Crossref | GoogleScholarGoogle Scholar |
Hodge, C. (1936). The anatomy and histology of the alimentary tract of the grasshopper, Melanoplus differentialis Thomas. Journal of Morphology 59, 423–439.
| The anatomy and histology of the alimentary tract of the grasshopper, Melanoplus differentialis Thomas.Crossref | GoogleScholarGoogle Scholar |
Hodge, C. (1939). The anatomy and histology of the alimentary tract of Locusta migratoria L. (Orthoptera: Acrididae). Journal of Morphology 64, 375–399.
| The anatomy and histology of the alimentary tract of Locusta migratoria L. (Orthoptera: Acrididae).Crossref | GoogleScholarGoogle Scholar |
Ibanez, S., Lavorel, S., Puijalon, S., and Moretti, M. (2013). Herbivory mediated by coupling between biomechanical traits of plants and grasshoppers. Functional Ecology 27, 479–489.
| Herbivory mediated by coupling between biomechanical traits of plants and grasshoppers.Crossref | GoogleScholarGoogle Scholar |
Judd, W. W. (1951). The proventriculus of some locusts of the family Eumastacidae (Orthoptera) with reference to its use in taxonomy. Canadian Journal of Zoology 29, 219–223.
| The proventriculus of some locusts of the family Eumastacidae (Orthoptera) with reference to its use in taxonomy.Crossref | GoogleScholarGoogle Scholar |
Lange, A. B., and Chan, K. (2008). Dopaminergic control of foregut contractions in Locusta migratoria. Journal of Insect Physiology 54, 222–230.
| Dopaminergic control of foregut contractions in Locusta migratoria.Crossref | GoogleScholarGoogle Scholar | 17953973PubMed |
Muralirangan, M. C., and Ananthadrishnan, T. N. (1974). Taxonomic significance of the foregut armature in some Indian Acridoidea (Orthoptera). Oriental Insects 8, 119–145.
| Taxonomic significance of the foregut armature in some Indian Acridoidea (Orthoptera).Crossref | GoogleScholarGoogle Scholar |
Patterson, B. D. (1984). Correlation between mandibular morphology and specific diet of some desert grassland Acrididae (Orthoptera). American Midland Naturalist 111, 296–303.
| Correlation between mandibular morphology and specific diet of some desert grassland Acrididae (Orthoptera).Crossref | GoogleScholarGoogle Scholar |
Porterfield, C. (2020). Apocalyptic pests: locust swarms hit Asia and South America, affecting millions. Forbes, 27 June 2020.
Roussi, A. (2020). Why gigantic locust swarms are challenging governments and researchers. Nature 579, 330.
| Why gigantic locust swarms are challenging governments and researchers.Crossref | GoogleScholarGoogle Scholar | 32184472PubMed |
Simpson, S. J. (2013). Mouthparts and feeding. In ‘The Insects: Structure and Function’. 5th edn. (Eds S. J. Simpson and A. E. Douglas.) pp. 15–45. (Cambridge University Press: Cambridge.)
Simpson, S. J., and Douglas, A. E. (2013). Nutrition. In ‘The Insects: Structure and Function.’ (Eds S. J. Simpson and A. E. Douglas) pp. 81–106. (Cambridge University Press: Cambridge.)
Teo, L. H., and Woodring, J. P. (1988). The digestive protease and lipase in the house cricket Acheta domesticus. Insect Biochemistry 18, 363–367.
| The digestive protease and lipase in the house cricket Acheta domesticus.Crossref | GoogleScholarGoogle Scholar |
Tietz, H. M. (1923). The anatomy of the digestive system of the Carolina locust (D. carolina, Linn.). Annals of the Entomological Society of America 16, 256–273.
| The anatomy of the digestive system of the Carolina locust (D. carolina, Linn.).Crossref | GoogleScholarGoogle Scholar |
Vosshall, L. B. (2020). Catching plague locusts with their own scent. Nature 584, 528–530.
| Catching plague locusts with their own scent.Crossref | GoogleScholarGoogle Scholar | 32788700PubMed |
Watson, G. S., Watson, J. A., and Cribb, B. W. (2017). Diversity of cuticular micro- and nanostructures on insects: properties, functions and potential applications. Annual Review of Entomology 62, 185–205.
| Diversity of cuticular micro- and nanostructures on insects: properties, functions and potential applications.Crossref | GoogleScholarGoogle Scholar | 28141960PubMed |
Woodring, J. (2017). The flow and fate of digestive enzymes in the field cricket, Gryllus bimaculatus. Archives of Insect Biochemistry and Physiology 95, e21398.
| The flow and fate of digestive enzymes in the field cricket, Gryllus bimaculatus.Crossref | GoogleScholarGoogle Scholar | 28631312PubMed |
Woodring, J., and Lorenz, M. W. (2007). Feeding, nutrient flow, and functional gut morphology in the cricket Gryllus bimaculatus. Journal of Morphology 268, 815–825.
| Feeding, nutrient flow, and functional gut morphology in the cricket Gryllus bimaculatus.Crossref | GoogleScholarGoogle Scholar | 17624929PubMed |
Zhou, S.-X. (2015). The role of the foregut in Orthoptera food processing. B.Sc.(Honours) Thesis, The Australian National University, Canberra, Australia.