The gut epithelium from feeding to fasting in the predatory soil mite Pergamasus longicornis (Mesostigmata: Parasitidae): one tissue, two roles

Abstract

A review of acarine gut physiology based on published narratives dispersed over the historical international literature is given. Then, in an experimental study of the free-living predatory soil mite Pergamasus longicornis (Berlese), quantitative micro-anatomical changes in the gut epithelium are critically assessed from a temporal series of histological sections during and after feeding on larval dipteran prey. An argued functional synthesis based upon comparative kinetics is offered for verification in other mesostigmatids. Mid- and hind-gut epithelia cell types interconvert in a rational way dependent upon the physical consequences of ingestion, absorption and egestion. The fasted transitional pseudo-stratified epithelium rapidly becomes first squamous on prey ingestion (by stretching), then columnar during digestion before confirmed partial disintegration (gut ‘lumenation’) during egestion back to a pseudo-stratified state. Exponential processes within the mid- and endodermic hind-gut exhibit ‘stiff’ dynamics. Cells expand rapidly (t1 / 2= 22.9–49.5 min) and vacuolate quickly (t1 / 2= 1.1 h). Cells shrink very slowly (t1 / 2= 4.9 days) and devacuolate gently (t1 / 2= 1.0–1.7 days). Egestive cellular degeneration has an initial t1 / 2= 7.7 h. Digestion appears to be triggered by maximum gut expansion—estimated at 10 min post start of feeding. Synchrony with changes in gut lumen contents suggests common changes in physiological function over time for the cells as a whole tightly-coupled epithelium. Distinct in architecture as a tissue over time the various constituent cell types appear functionally the same. Functional phases are: early fluid transportation (0–1 h) and extracellular activity (10–90 min); through rising food absorption (10 min to > 1 day); to slow intracellular meal processing and degenerative egestive waste material production (1 to > 12 days) much as in ticks. The same epithelium is both absorptive and degenerative in role. The switch in predominant physiology begins 4 h after the start of feeding. Two separate pulses of clavate cells appear to be a mechanism to facilitate transport by increasing epithelial surface area in contact with the lumen. Free-floating cells may augment early extracellular lumenal digestion. Possible evidence for salivary enzyme alkaline-related extra-corporeal digestion was found. Giant mycetome-like cells were found embedded in the mid-gut wall. Anteriorly, the mid-gut behaves like a temporally expendable food processing tissue and minor long-term resistive store. Posteriorly the mid-gut behaves like a major assimilative/catabolic tissue and ‘last-out’ food depot (i.e., a ‘hepatopancreas’ function) allowing the mite to resist starvation for up to 3.5 weeks after a single meal. A ‘conveyor-belt’ wave of physiology (i.e., feeding and digestion, then egestion and excretion) sweeps posteriorly but not necessarily pygidially over time. Assimilation efficiency is estimated at 82%. The total feeding cycle time histologically from a single meal allowing for the bulk of intracellular digestion and egestive release is not 52.5 h but of the order of 6 days (≡ 0.17 total gut emptyings per day), plus typically a further 3 days for subsequent excretion to occur. Final complete gut system clearance in this cryptozooid may take much longer (> 15 days). A common physiology across the anactinotrichid acarines is proposed. A look to the future of this field is included.