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. Midand hind-gut epithelia cell types interconvert in a rational way dependent upon the physical consequences of ingestion, absorption and egestion. The fasted transitional pseudostratified 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 Extended author information available on the last page of the article Research Council grant B/77307818 at Liverpool John Moores University. Thanks go to Susan Bjornson (then at University of Alberta, Canada) for advice on invertebrate sporozoans and Don E Johnston (Ohio Sta...

Metabarcoding analysis of different portions of the digestive tract of scorpions (Scorpiones, Arachnida) following a controlled diet regime shows long prey DNA half‐life

“…Since our tested scorpions have been maintained exclusively on a diet of crickets prior to the beginning of the treatment, cricket permanence in the mid‐gut and its consequent detection may be a result of prolonged exposure to that prey type in the past. Alternatively, as already observed in mites, the mid‐gut is readily filled with food along its length, but the distribution of nutrients in the absorbing and storing tissues is not totally synchronous, and the most caudal portions of the mid‐gut may be the last to be emptied (Bowman, 2017, 2019). This possibility is corroborated by the detection of asynchronous digestive processes across diverticula in scorpions fasting for 1 month (Goyffon & Martoja, 1983).…”

Feeding design in free-living mesostigmatid chelicerae (Acari: Anactinotrichida)

“…However, this is useful as there are limited ways to subdivide the carnivore niche for any broad analysis (the other factors being prey size and the proportion of foodstuff types consumed; Van Valkenburgh 2007). In both cases tissue maceration i.e., food softening by soaking in an extracorporeal liquid is assumed before ingestion (Bowman 2019).…”

“…Moreover in situations facing vertebrates carnivores (Van Valkenburgh 2007) where rapid ingestion is favoured (such as between litter-mates or adults feeding together on a kill), selection should favour the evolution of a longer blade and greater bite force. Free-living mesostigmatids ingest very rapidly (Bowman 2019) so a pressure for this change probably exists similarly. Note that active consumption rates increases with sociality in carnivorous vertebrates (Wilmers and Stahler 2002).…”

“…Are there acarine equivalents of crustacean 'pectinate claws' (Tshudy and Sorhannus 2000)? These almost impossibly long slender-fingered chelae armed with pectinate Vázquez et al (2016) and, the gnathotectum etc then all would facilitate liquid recycling needed for predation on watery prey (Bowman 2014(Bowman , 2017b(Bowman , 2019 when burrowing, delving into and excavating soil pores for food or shelter. Coxae in arachnids are discussed in Van der Hammen (1977a) where he points out that some of the most primitive arachnid members have been found in the deeper layers of soil.…”

“…For instance, the long lanceolate ventrally curved gnathotectum of eviphidids may assist in the holding or perhaps the piercing of their nematode prey. Salivary enzymes (Bowman 2019) delivered by stylets (Evans 1992;Krantz and Walter 2009) facilitate prey liquefaction. The gnathotectum above the chelicerae together with the palps (Bowman 1984), plus the tritosternum and gnathosomal groove (Wernz and Krantz 1976) can maintain a fluid cylinder extended around the hypostome and mouth (Alberti and Coons 1999).…”