The gut epithelium from feeding to fasting in the predatory soil mite Pergamasus longicornis (Mesostigmata: Parasitidae): one tissue, two roles
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...
| Main Author: | |
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| Format: | Journal article |
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Springer
2019
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| _version_ | 1797053176710430720 |
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| author | Bowman, C |
| author_facet | Bowman, C |
| author_sort | Bowman, C |
| collection | OXFORD |
| description | 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 suggest 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 - >1 day); to slow intracellular meal processing and degenerative egestive waste material production (1 - >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. |
| first_indexed | 2024-03-06T18:40:20Z |
| format | Journal article |
| id | oxford-uuid:0ca764ae-c1c8-4a57-b303-6bd1495673cc |
| institution | University of Oxford |
| last_indexed | 2024-03-06T18:40:20Z |
| publishDate | 2019 |
| publisher | Springer |
| record_format | dspace |
| spelling | oxford-uuid:0ca764ae-c1c8-4a57-b303-6bd1495673cc2022-03-26T09:36:13ZThe gut epithelium from feeding to fasting in the predatory soil mite Pergamasus longicornis (Mesostigmata: Parasitidae): one tissue, two rolesJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:0ca764ae-c1c8-4a57-b303-6bd1495673ccSymplectic Elements at OxfordSpringer2019Bowman, CA 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 suggest 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 - >1 day); to slow intracellular meal processing and degenerative egestive waste material production (1 - >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. |
| spellingShingle | Bowman, C The gut epithelium from feeding to fasting in the predatory soil mite Pergamasus longicornis (Mesostigmata: Parasitidae): one tissue, two roles |
| title | The gut epithelium from feeding to fasting in the predatory soil mite Pergamasus longicornis (Mesostigmata: Parasitidae): one tissue, two roles |
| title_full | The gut epithelium from feeding to fasting in the predatory soil mite Pergamasus longicornis (Mesostigmata: Parasitidae): one tissue, two roles |
| title_fullStr | The gut epithelium from feeding to fasting in the predatory soil mite Pergamasus longicornis (Mesostigmata: Parasitidae): one tissue, two roles |
| title_full_unstemmed | The gut epithelium from feeding to fasting in the predatory soil mite Pergamasus longicornis (Mesostigmata: Parasitidae): one tissue, two roles |
| title_short | The gut epithelium from feeding to fasting in the predatory soil mite Pergamasus longicornis (Mesostigmata: Parasitidae): one tissue, two roles |
| title_sort | gut epithelium from feeding to fasting in the predatory soil mite pergamasus longicornis mesostigmata parasitidae one tissue two roles |
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