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

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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 (\(t_{1/2}=\) 22.9–49.5 min) and vacuolate quickly (\(t_{1/2}=\) 1.1 h). Cells shrink very slowly (\(t_{1/2}=\) 4.9 days) and devacuolate gently (\(t_{1/2}=\) 1.0–1.7 days). Egestive cellular degeneration has an initial \(t_{1/2}=\) 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 (\(\equiv 0.17\) 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.
Statistical analysis. Upper: minimum spanning circle mapping of inter-point distances (di,j\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$d_{i,j}$$\end{document}) between the complete histologically scored character data at each time point from feeding to fasting in Pergamasus longicornis. Uses all cellular data herein plus that from Bowman (2014, 2017a, b). Distance around circle is reciprocally weighted Jacquard similarity index between adjacent sequentially displayed points, confirming four phases. (D) = digestion phase. (I, E) = ingestion, egestion/excretion phase. (O) = osmoregulatory (‘coxal droplet’) phase. Physiological time course for partially overlapping phases should be read anti-clockwise (I→O→D→E)\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$(\hbox {I}\rightarrow \hbox {O}\rightarrow \hbox {D}\rightarrow \hbox {E})$$\end{document}. Labels are in min or h (see Materials and Methods). Dot is used to denote different replicates for clarity. Greyed out label for 6h is at peak of production of globular material in the gut lumen (Bowman 2017a). Greyed out label for aberrant result at 366 h is during starvation. Middle: left: scores plot from divergences SVD (black circles = reference t=0\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$t=0$$\end{document}. Middle: right: loadings plot from SVD. Small open circles = lag terms. Note that to the right and down direction are: black squares = cell characteristics; grey squares = granular and globular food; crosses = expansion/contraction and lumen score. Note to the left and up direction are: X = other and membraneous material in lumen; grey stippled square = refractive grains; open circle = Malpighian tubule expansion and guanine. Middle: central: Ln(time) contours over SVD scores plot showing time passes anticlockwise (dark→pale\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$\hbox {dark}\rightarrow \hbox {pale}$$\end{document}, black ≡\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$\equiv $$\end{document} initial starved state, white ≡\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$\equiv $$\end{document} starving. Lower: scores plot from SVD with line showing time course of changes for each gut region overlain on anatomy from Bowman (2014). Note ‘echo’ or extra cycle (cf. Fig. 18, middle) in posterior gut caeca—‘slow’ digestion before fasting/starvation?
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