Histological and histochemical analysis of the gastrointestinal tract of the common pipistrelle bat (Pipistrellus pipistrellus)

Abstract

Bats have a very high mass-specific energy demand due to small size and active flight. European bat species are mostly insectivorous and the morphology of the gastrointestinal (GI) tract should be adapted accordingly. This study investigated the general anatomy by histology and the function by analysing carbohydrate distribution in particular of the mucus of the GI tract of the insectivorous bat Pipistrellus pipistrellus. The GI tracts of three individuals were dissected, fixed in formaldehyde, and embedded in paraffin wax. The tissues and cells of the GI tract of P. pipistrellus were analysed by classical (acid alizarin blue, haematoxylin-eosin, and Masson Goldner Trichrome), histochemical (periodic acid-Schiff, Alcian blue at pH 2.5) and lectin histochemical (lectins WGA and HPA) staining procedures. The GI tract of P. pipistrellus is organised into the typical mammalian layers. The short, narrow, and thin-walled esophagus is simple with a folded stratified squamous epithelium without glands but mucous surface cells secreting neutral mucus. The stomach is globular shaped without specialisation. Mucous surface cells produced neutral mucus whereas neck and parietal cells secreted a mixture of neutral and acid mucus. Chief cell surface was positive for N-acetylglucosamine and the cytoplasm for N-acetylgalactosamine residues. The intestine lacked a caecum and appendix. The small intestine was divided into duodenum, jejunum-ileum and ileum-colon. The epithelium consisted of columnar enterocytes and goblet cells. The large intestine is short, only represented by the descending colon-rectum. It lacked villi and the mucosa had only crypts of Lieberkühn. Towards the colon-rectum, goblet cells produced mucus with N-acetylglucosamine residues increasing in acidity except in colon-rectum where acidity was highest in the base of crypts. Along the tube the surface of enterocytes was positive for N-acetylglucosamine and N-acetylgalactosamine. All over the mucus filling the lumen of the GI tract was positive for N-acetylglucosamine and increased in acidity in all parts except of the stomach.In conclusion, the simple GI tract showed an anatomical reduction of tissue enabling for a short retention time and a reduction of the load carried during flight: short GI tract, lack of lymphoid tissue, missing of glands in certain regions, and a distinct pattern of mucus distribution, indicating different physiological functions of these areas. The GI tract of P. pipistrellus was typical for an insectivorous species probably representing the ancestral condition.

Ecology and Host Identity Outweigh Evolutionary History in Shaping the Bat Microbiome

“…Flight is an energetically demanding form of locomotion that requires the animal to have a digestive system that meets its high metabolic needs with a gut that is low in weight. Relative to most nonflighted mammals, bats have comparatively smaller gastrointestinal (GI) tracts, reduced intestinal tissue, and smaller digestive loads that help to minimize flight mass (60,62,64,65). Bats also have relatively streamlined GI tract design, regardless of dietary niche, that lacks a cecum and appendix (66), but still achieves high digestive efficiencies (65,67).…”

“…Relative to most nonflighted mammals, bats have comparatively smaller gastrointestinal (GI) tracts, reduced intestinal tissue, and smaller digestive loads that help to minimize flight mass (60,62,64,65). Bats also have relatively streamlined GI tract design, regardless of dietary niche, that lacks a cecum and appendix (66), but still achieves high digestive efficiencies (65,67). This phenomenon is potentially explained by the ability of small birds and bats to meet high metabolic demands via paracellular nutrient absorption (61).…”

Chiroptera

“…In general, bats have a short gastrointestinal (GI) tract and rapid GI transit time, likely an adaptation for flight (Strobel et al, 2015). The stomachs are relatively simple in insectivorous bats but may be larger and more complex in some frugivorous and nectarivorous bats (Stevens and Hume, 1995).…”

Histochemistry in biology and medicine: a message from the citing journals

“…As a journal of functional cytology, the European Journal of Histochemistry has traditionally published many papers on cell and tissue biology in a variety of Vertebrate and Invertebrate species. After a relative decrease in 2013 and 2014, 103-115 in the present year more than 20% of the published papers were on these subjects, 116-126 thus demonstrating that histochemical techniques are powerful tools for properly describing cell and tissue organization as well as functional microanatomy in different taxa of still poorly described organisms. In a comparative perspective, the histochemical evidence, in parallel with molecular data on protein and DNA, may help to elucidate the origin and evolution of cell and tissue physiology.…”