Feeding, nutrient flow, and functional gut morphology in the cricket Gryllus bimaculatus

Abstract

The flow of nutrients through the digestive tract of Gryllus bimaculatus is regulated by the proventriculus, which effectively triturates the partially digested food coming from the crop and shoves the mushy nutrient mass into the space between the paired caeca. The many folds at the base of the caeca form a sieve, and only fine food particles (4-10 microm) and fluids in the mush are filtered under pressure (produced by proventricular peristalsis) into the caeca. Combined with the release of enzymes in the caeca and the influx of water, the caeca are rapidly inflated on day 1 after the terminal molt. The remaining, mostly undigested food is shoved into a tube formed by the peritrophic membrane, which is first formed at the anterior end of the ventriculus. A mucous membrane (peritrophic gel) covers the caecal epithelium, and seems to merge with the true peritrophic membrane at the beginning of the ventriculus. The Type I peritrophic membrane is dragged posteriorly through the entire ventriculus and ileum by the posterior movement of the food bolus, which is shoved posteriorly at a rate of 6 mm/h by proventricular pressure. The growth rate of the peritrophic membrane is about 3 mm/h. Peristalsis does not occur in the midgut or ileum; the muscles in these regions function solely to counteract the internal pressure produced by the proventriculus. The exo- and endoperitrophic space in newly molted animals is open and fluids can flow in both directions. The endoperitrophic space becomes filled on day 1, and leads to a great reduction of the exoperitrophic space. In the ileal pouch (exoperitrophic space) the peritrophic membrane separates the mass of bacteria from the waste bolus within the endoperitrophic space. Feathery bristles arising from the cuticular covering of the finger-like invaginations of the ileal wall hold most of the bacterial mass in place. The crop weight decreases from day 1 to day 3 as the weight of caeca, ventriculus, and ileum increases. After day 3, food uptake and the weight of the entire gut system decrease in female crickets, partly in response to space restrictions in the abdomen caused by rapid ovarial growth.

Spatial Structure of the Mormon Cricket Gut Microbiome and its Predicted Contribution to Nutrition and Immune Function

“…In some insects, specialized midgut crypts provide niches that microbes colonize (Kikuchi et al, 2005; Bistolas et al, 2014). While the gastric caeca ( Figure 1 ) have not been reported as an important site for microbial colonization in other orthopterans (Hunt and Charnley, 1981; Woodring and Lorenz, 2007), future studies should explore whether microbial communities in the caeca are similar in abundance and composition to the rest of alimentary tract.…”

“…The foregut serves as the entry point for food, where it is stored in the crop before passing through the proventriculus, a valve that can also be modified to mechanically filter food (Woodring and Lorenz, 2007; Douglas, 2013) and even microbes (Lanan et al, 2016). Digestion and absorption of nutrients begins at the midgut, which, in some species, contains specialized crypts that house microbes that aid in insect nutrition (Kikuchi et al, 2005; Bistolas et al, 2014).…”

“…Malpighian tubules permeate the anterior hindgut, excreting nitrogenous waste and other solutes from the hemocoel that can provide nutrients for dense populations of microbes (Bignell, 1984). In some species, dense bristle-like structures in the ileum (Woodring and Lorenz, 2007) and rectal papillae (Hunt and Charnley, 1981) provide attachment sites for bacteria, some of which fix nitrogen (Tai et al, 2016), degrade recalcitrant plant polymers (Kaufman and Klug, 1991; Engel and Moran, 2013), and prevent infection (Dillon and Charnley, 2002). …”

SECRETION OF LIPASES IN THE DIGESTIVE TRACT OF THE CRICKET Gryllus bimaculatus

“…Since the volume of each region for 1‐ to 2‐day‐old crickets is known (above), we calculated the entire TLA for each region (Fig. ), and found the total activity of the entire gut was 524 nmol pNP/30 m. A fairly steady feeding and fecal production was observed in G. bimaculatus (Woodring and Lorenz, ). Therefore, we could estimate that at a steady flow rate in the gut about 10% of the TLA in the total gut is found in the crop, 70% in the caecae, 18% in the ventriculus, only 3% in the ileum.…”

“…Even less information is available on the secretion of lipases. In Manduca sexta , secretion of PLA 2 is regulated by feeding, with a set baseline rate (Rana and Stanley, ), and in G. bimaculatus , the secretion of total lipase was likewise related to feeding, with a basal secretion rate in unfed animals (Woodring et al., ). In G. bimaculatus , the activity of trypsin and carbohydrases is reduced in unfed females, but it is never reduced to zero secreted activity (Weidlich et al., , ).…”