Gut contents, digestive half-lives and feeding state prediction in the soil predatory mite Pergamasus longicornis (Mesostigmata: Parasitidae)

Abstract

Mid- and hind-gut lumenal changes are described in the free-living predatory soil mite Pergamasus longicornis (Berlese) from a time series of histological sections scored during and after feeding on fly larval prey. Three distinct types of tangible material are found in the lumen. Bayesian estimation of the change points in the states of the gut lumenal contents over time is made using a time-homogenous first order Markov model. Exponential processes within the gut exhibit ‘stiff’ dynamics. A lumen is present throughout the midgut from 5 min after the start of feeding as the gut rapidly expands. It peaks at about 21.5 h–1.5 days and persists post-feeding (even when the gut is contracted) up until fasting/starvation commences 10 days post start of feeding. The disappearance of the lumen commences 144 h after the start of feeding. Complete disappearance of the gut lumen may take 5–9 weeks from feeding commencing. Clear watery prey material arrives up to 10 min from the start of feeding, driving gut lumen expansion. Intracellular digestion triggered by maximum gut expansion is indicated. Detectable granular prey material appears in the lumen during the concentrative phase of coxal droplet production and, despite a noticeable collapse around 12 h, lasts in part for 52.5 h. Posterior midgut regions differ slightly from anterior regions in their main prey food dynamics being somewhat faster in processing yet being slightly delayed. Posterior regions are confirmed as Last-In-Last-Out depots, anterior regions confirmed as First-In-First-Out conveyor belt processes. Evidence for differential lability of prey fractions is found. A scheme is presented of granular imbibed prey material being first initially rapidly absorbed ( = 23 min), and also being quickly partly converted to globular material extra-corporeally/extracellularly ( = 36 min)—which then rapidly disappears ( = 1.1 h, from a peak around 4 h). This is then followed by slow intracellular digestion ( = 6.9 h) of the resultant resistant prey residue matching the slow rate of appearance of opaque pre-excretory egestive refractive grains (overall = 4.5 days). The latter confirmed latent ‘catabolic fraction’ (along with Malpighian tubule produced guanine crystals) drives rectal vesicle expansion as ‘faeces’ during the later phases of gut emptying/contraction. Catabolic half-lives are of the order of 6.3–7.8 h. Membraneous material is only present in the lumen of the gut in starving mites. No obvious peritrophic membrane was observed. The total feeding cycle time may be slightly over 52.5 h. Full clearance in the gut system of a single meal including egestive and excretory products may take up to 3 weeks. Independent corroborative photographs are included and with posterior predictive densities confirm the physiological sequence of ingestion/digestion, egestion, excretion, defecation, together with their timings. Visually dark midguts almost certainly indicate egestive refractive grains (xanthine?) production. Nomograms to diagnose the feeding state of P. longicornis ...

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

“…Lumen presence/absence mean score from Bowman (2017a)-no symbol and black dashed dotted smoothed (fifth order polynomial) trend line. Marbled lower grey line is granular contents in the lumen (Bowman 2017b). Solid hashed line ending with X = presence of 'coxal droplets' (Bowman 2014).…”

“…Mid-and endodermic hind-gut cell types are expected to: wax and wane with high functional activity (like in phytoseiids-Akimov and Starovir 1978;Starovir 1982); then differentiate and interconvert (like in argasids- El Shoura 1988); as the pergamasid gut epithelium changes its form during the process of feeding and digestion on a larval dipteran prey. Opisthosomal colour itself changes in P. longicornis over feeding and excretion (Bowman 2017b), much as the weights of ticks (and optical densities of tick extracts) changes in concert with the colour of their caecal contents (Fig. 3 in Arthur 1965;Fig.…”

“…Consilience of physiological staging in determining any digestive 'age' grade during feeding to fasting is powerful evidence that any explanation is well founded rationally (for example see the use of heme and protein levels in ticks- Reid and Boid 1984). So, epithelial evidence of pergamasid digestion should be contemporaneous with any observed changes of ingested food (Bowman 2017b), and, epithelial evidence of egestion should be contemporaneous with observed changes in waste contents (Bowman 2017a, b). Thus this paper in particular seeks quantitatively:…”

“…(c) Check for a 'digestive switch' around 2 h and an 'egestive' switch around 4 h (Bowman 2014, 2017b), (d) Recheck if food elimination is slower in the anterior gut compared to the posterior parts (i.e., the antithesis of hypothesis (iv) in Bowman 2017b), (e) Check if cellular processes are 'stiff', and how stiff they are compared to gut expansion/ contraction (Bowman 2014), Malpighian processes (Bowman 2017a), and lumenal content processing (Bowman 2017b), (f) Check 'hypothesis (viii)' from Bowman (2017b) as to just what is a good indicator of starvation in this arachnid, via a critical assessment of all cell types and their vacuolation quantitatively over time. These will be denoted as 'Check (a)' through to 'Check (f)' in the "Discussion"for easy cross reference.…”

“…For gut 'Lumenation' see Fig. 20 and "Discussion", data from Bowman (2017b) ‡ Each phase separately fitted to data-simultaneous kinetic models for appearance and disappearance gave inappropriate estimates *Trimmed to examine consistency and in order to compare to 20-120 min interval in Bowman (2017b) **Extended to give slowest possible decline based upon data (see text) † Data and time-windows for kinetic modelling from Bowman 2014 ell 1964). Only traces were found lumenally.…”