Evaluation of the morphological adaptations of the small intestine of the African pied crow (Corvus albus) The Journal of Basic & Applied Zoology (2016) 75, 54–60 HO ST E D BY The Egyptian German Soci[.]
The Journal of Basic & Applied Zoology (2016) 75, 54–60 H O S T E D BY The Egyptian German Society for Zoology The Journal of Basic & Applied Zoology www.egsz.org www.sciencedirect.com Evaluation of the morphological adaptations of the small intestine of the African pied crow (Corvus albus) Okpe Chidozie Godwin, Abiaezute Nwabugwu Clifford *, Adigwe Agatha Department of Veterinary Anatomy, Faculty of Veterinary Medicine, University of Nigeria, Nsukka, Nigeria Received 31 March 2016; revised 29 June 2016; accepted 11 December 2016 Available online 11 January 2017 KEYWORDS African pied crow; Small intestine; Crypts of lieberkuhn; Goblet cell; Microvilli; Villi Abstract The morphology and morphometry of the small intestine of the Adult African pied crow in a tropical habitat was studied Fifteen African pied crows used in this study revealed modification of the jejunum into centripetal and centrifugal cone shaped spiral coils The weight and length of jejunum was significantly greater (p < 0.05) than those of duodenum and ileum respectively Histologically, the tunica mucosa in all the segments was modified into villi which showed wavy and anastomosing configurations in the jejunum Each villus was lined by simple columnar epithelium with numerous goblet cells The length, population and surface area of villi in the jejunum was significantly (p < 0.05) higher than those of the duodenum and ileum respectively while the population of goblet cells were significantly higher (p < 0.05) in the ileum compared to the duodenum and jejunum The bases of the villi were modified into the crypts of lieberkuhn which together with numerous mucosal glands are located in the connective tissue of the lamina priopria The lamina muscularis mucosae separated the lamina propria from the thin submucosa in the walls of the three segments The tunica muscularis was significantly thicker (p < 0.05) in the jejunum than in the ileum and duodenum respectively The morphological modifications probably maximize space for efficient absorption and reduction of digestive load Ó 2016 The Egyptian German Society for Zoology Production and hosting by Elsevier B.V This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/) Introduction The African pied crow is commonly found in close association with human settlement in African countries characterized by a * Corresponding author E-mail addresses: godwin.okpe@unn.edu.ng (C.G Okpe), nwabugwu.abiaezute@unn.edu.ng (N.C Abiaezute), adigweagatha@gmail com (A Adigwe) Peer review under responsibility of The Egyptian German Society for Zoology glossy black plumage interrupted by a large area of white feathering from the shoulder down to the lower breast (Hartwig and Morel, 1997) The pied crow, an omnivore is a voracious eater capable of consuming more than half its own body weight of food per day (Allen, 1968) Being a carinate as other flying birds, it is expected that they should have reduced intestinal volume and reduced digestive load, an adaptation to minimize energetic cost of flying and manoeuvrability (Guillemette, 1994; Norberg, 1995; Nudds and Bryant, 2002) To meet their metabolic needs while remaining as light weighted as possible, flying birds operate with a reduced diges- http://dx.doi.org/10.1016/j.jobaz.2016.12.002 2090-9896 Ó 2016 The Egyptian German Society for Zoology Production and hosting by Elsevier B.V This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/) Morphological adaptations of the small intestine of the African pied crow tive capacity, compared with that of non flying mammals (Lavin et al., 2008) Environmental factors including type and quality of feed and dietary habits influences the anatomy and size of avian digestive tracts (Kehoe and Ankner, 1985; Jordano, 1987; Dz iała-Szczepan´czyk and Wesołowska, 2008) The small intestine is short and slightly coiled in most meat eating birds, but longer and highly coiled in herbivorous and omnivorous bird (Casotti, 2001) The central role of the small intestine in digestion and absorption has been extensively reported (Riesenfeld et al., 1980; Klasing, 1998; Denbow, 2000; Lorenzoni, 2010) Intestinal absorption process probably evolved differently in avian This may be an explanation to variations in the digestive efficiency observed in the avian species It has been opined that variations in the absorptive epithelium are responsible for the differences in absorptive potentials of birds A larger small intestinal volume or nominal surface area is presumed to allow more surface area over which nutrients can be digested and absorbed (Lavin et al., 2008) Small intestines of birds have been shown to vary in length and structure depending on the diet of the species (Casotti, 2001; Lavin et al., 2008) Birds posses short gut retention time for food, however, this appear to be compensated by increased mucosal surface area achieved by greater villus area (Lavin et al., 2008) Reports on the morphology and morphometry of the small intestine of some species of birds are available (Casotti, 2001; Działa-Szczepan´czyk and Wesołowska, 2008; Lavin et al., 2008; Wang and Peng, 2008; Igwebuike and Eze, 2010; Hamdi et al., 2013) However, there is paucity of information on the morphology and morphometry of the small intestine of the African pied crow The present study was designed to provide further information on the gross morphology, histology and morphometry of small intestine of Adult African pied crow in a tropical Nigerian habitat Materials and methods Gross preparation Fifteen African pied crows used for this study were obtained from the Zoological garden, University of Nigeria Nsukka The birds were weighed and sacrificed by euthanasia with an overdose of intravenous injection of phenobarbitone following the guidelines given by the Ethics Committee of the Veterinary Faculty The small intestine was dissected out, drained of food materials remaining in the lumen by washing with lactated Ringer’s solution, weighed and the length measured The duodenum (pancreatic loop), Jejunum (from pancreatic loop to the Meckel’s diverticulum), ileum (from Meckel’s diverticulum to the ileocecal junction) were measured and weighed The weight– length ratios of the segments were calculated as indicator of intestinal density as described by Taylor and Jones (2004) Morphometric data of the organ weight and length were expressed per kilogram body weight 55 in xylene, and embedded in paraffin wax lm thick sections were obtained and stained with haematoxylin and eosin Some of the sections from the different segments of the small intestine were stained with Periodic Acid Schiff (PAS) and Alcian Blue respectively The stained sections were examined using (MoticÒ China B1 Advanced Series) microscope Micrographs of the sections were captured with Moticam Camera 1000 (1.3 M Pixel USB 2.0) attached to a computer Histometry The numbers of villi on each segment of the small intestine were counted The mean number of goblet cells per villus was counted and the villus area obtained from villi per tissues per slide Twenty-four measurements were used to obtain a mean number of goblet cells per bird The goblet cell number per villus area was calculated and normalized using the natural log as described by Walk et al (2011) With a standardized eye piece micrometer, longitudinally or sagittally orientated villi were randomly selected, the mean villus height (measured from the base to the top) and width (at half height) were determined as described by Jaeger et al (1990) and Iji et al (2001) The villus area was determined as a product of villus height and width The depth of the crypts and the thickness of the tunica muscularis were also measured using the same standardized eye piece micrometer Statistical analysis The means and standard errors of the mean (mean ± SEM) of the gross biometric and histometric data were calculated They were analysed using analysis of variance (ANOVA) and Duncan New Multiple Range Test Significance was accepted at probability level of p < 0.05 Results Morphology Grossly, the small intestine of the African pied crow consisted of the duodenum, jejunum and ileum (Fig 1) The duodenum Histological preparation Samples taken from segments of the small intestine (duodenum, jejunum and ileum) were fixed by immersion in Bouin’s fluid for 16 h, post fixed in 10% buffered formalin, later dehydrated in ascending grades of ethanol concentrations, cleared Figure Small intestine of the African pied crow showing the duodenal loop (DU) enclosing the pancreas (arrow), the ileum (IL), the centripetal and centrifugal coils of the jejunum (SC) Note the sigmoid flexure (SF) of the jejunum that formed the apex of the cone 56 arose from the pylorus and formed a characteristic U shaped loop that encircled the pancreatic tissue between its proximal descending and distal ascending parts Within the ascending duodenum were two pancreatic ducts and two bile ducts that emptied into its distal end The end of the duodenal loop marked the beginning of the jejunum The jejunum was the longest segment of the small intestine and appeared as a cone shaped spiral coils of centripetal and centrifugal parts The centripetal part formed the outer coils, while the centrifugal part formed the inner coils A third short part of the jejunum had the shape of a sigmoid flexure and formed the apex of the cone The short ileum continued from the jejunum and terminated at a junction of the caeca to the large intestine The mean weight of the small intestine expressed as a percentage body weight was 3.30 ± 0.51 The weight, length and relative organ weight of the duodenum, jejunum and ileum are as shown in the table Histology The wall of the small intestine consisted of four main tunics; tunica mucosa, tunica submucosa, tunica muscularis and tunica serosa The tunica mucosa in the three segments of the small intestine was modified into numerous longitudinal finger-like mucosal projections, villi, which extended into the intestinal lumen These surface evaginations consisted of lining surface epithelium, goblet cells and the underlining connective tissue of the lamina propria The villi of jejunum were long and wavy, exhibiting branching pattern which anastomosed with each other forming a labyrinthine configuration (Fig 2) Those villi located at the duodenum and ileum showed typical fingerlike projections (Fig 3) Each villus in all segments was lined by a simple columnar epithelium with striated apical border interspersed with numerous goblet cells (Fig 4) The mucosa of all three segments of the small intestine showed a strong bluish and magenta colouration of the goblet cells to the Alcian blue and PAS staining techniques respectively (Figs and 6) These reactions were seen in the goblet cells of the villi and the crypts of lieberkuhn The base of each villus showed numerous simple or branched tubular invaginations of the epithelium into the underlying connective tissue of the lamina propria to form tubular glands (crypts of lieberkuhn) (Fig 3) The mean Figure Cross section of the jejunum showing the anastomosing villi (V), mucosal glands (MG) in the lamina propria and the tunica muscularis (TM) H&E 40 C.G Okpe et al Figure Cross section of the ileum of African pied crow showing villi (V), the mucosal glands (MG), the lymphoid nodule (LN) and crypts of lieberkuhn (arrow) within the lamina priopria (LP) Note the muscularis mucosae (MM) and the thin submucosa (SM), the inner circular (CM) and outer longitudinal (LM) smooth muscles and the tunica serosa (arrow heads) Also note the blood vessels (BV) within the tunica muscularis H&E stain Figure Photomicrograph of the villi showing the simple columnar epithelium containing numerous goblet cells (G) Note the core of the villi containing loose connective tissue (CT) PAS stain Figure Cross section of the jejunum showing the branching anastomosing mucosal villi (V) with numerous Alcian Blue positive goblet cells (G) Note the mucosal glands (MG) Alcian Blue stain Morphological adaptations of the small intestine of the African pied crow length, width, areas and population of villi in the three segments of the small intestine are presented in the table Likewise, the population of the goblet cells and the depth of crypts of lieberkuhn in each segment are shown in the table The villus height/crypt depth ratio was highest in the jejunum and least in the ileum The lamina propria contained numerous mucosal glands and its connective tissue extended into and formed the cores of the villi (Fig 4) The results of this study also showed that the lamina muscularis mucosae of the small intestine of the African pied crow separate the lamina propria from the thin submucosa in the walls of the three segments The tunica muscularis consists of two layers of smooth muscle fibers in all segments of the small intestine (Figs and 6) The inner layer is thick and circularly oriented, while the outer layer is thin and longitudinally oriented The tunica muscularis was significantly (p < 0.05) thicker in the jejunum than in the ileum and duodenum respectively (Table 1) Numerous blood vessels and nerve plexuses were present within the tunica muscularis of the three segments of the small intestine of the African pied crow A thin layer of loose connective tissue covered the tunica muscularis as the tunica serosa with its external surface lined by a simple squamous epithelium Apart from the structural differences observed in the histology of the villi in the ileum, qualitative histology of the segments was similar Discussion The present study showed that the small intestine of the African pied crow was similar to other avian species to the extent that it consisted of duodenum, jejunum and the ileum but differed in the arrangement of these segments The loop and spiral coil arrangements of the duodenum and jejunum respectively had been described in pigeon (McLelland, 1990; Dyce et al., 2002) This loop and spiral arrangements of the small intestine of the African pied crow appear to be an adaptation to contain the length of the intestine within relatively small available space in the abdominal cavity The looping and spiralling of the intestine, increases the route of the ingesta, surface areas of intestine and contact time of ingesta and mucosal surface of the intestine, thus enhancing digestion Figure Cross section of the duodenum showing the villi (V) with numerous PAS positive goblet cells (G), mucosal glands (MG), the muscularis mucosae (MM), the inner circular smooth muscles (CM), outer longitudinal smooth muscles (LM), blood vessels (arrow) and the tunica serosa (TS) PAS stain 57 and absorption of nutrient (Banks, 1993) Igwebuike and Eze (2010) similarly opined that the spirally coiled jejunum was an adaptation of this bird for maximal utilization of space The mass of the small intestine as recorded in the present study is similar to those recorded for other avian species of similar size (Bailey et al., 1997; Yang et al., 2013) However the relative weight of 3.30% in this study was heavier than that of many high flying birds Barton and Houston (1993) reported a relative body weight of 0.63%, 0.42%, 0.99% and 1.26% for sparrow hawk, Barn owl, Buzzard and Tawny owls respectively The variations in the percentage of relative weight are probably due to the fact that African pied crows are omnivores and capture preys in a passive hunting mode, not depending solely on high speed powerful flight as done by the carnivorous birds This view is supported by report of Barton and Houston (1994, 1996) More also, Pied crow spends most of its time on the ground scavenging for food, thus little energy is spent on flying and manoeuvrability as it has been reported that small intestinal volume and mass as recorded in high flying birds is to minimize cost associated with flight (Nudds and Bryant, 2002) Of the three segments of the small intestine, the jejunum had a relatively greater weight The increased weight of the jejunum could be attributed to the length of the jejunum, and increased thickness of the tunica muscularis as reported in the present study The length of the small intestine of the pied crow is about 68 cm Intestinal lengths of 56 cm and 65 cm was earlier reported in quail and pigeon respectively (Hena et al., 2012) The disparity could be as a result of variations in weight of the birds, flight capability and eating habits as bird’s small intestines are known to change in length, structure and digestive efficiency depending on diet (Savory and Gentle, 1976; Piersma et al., 1993; Hilton et al., 1999; Hamdi et al., 2013) Moreover, the African pied crow being an omnivore, the small intestinal length was longer than the carnivorous birds (Hamdi et al., 2013) In the pied crow, the jejunum constituted the longest part of the small intestine This is suggestive of an increased surface area and improved absorption efficiency (Banks, 1993) Similar finding has been reported in other bird species such as ostrich and chicken (Soriano et al., 1993; Wang and Peng, 2008; Duritis and Mugurevics, 2011) In addition to the gross morphological variations between the segments of the small intestine, histological observations demonstrated variations in the mucosal surfaces and tunica muscularis The wall of the small intestine of the African pied crow has four layers of tissues typical of avian species (Banks, 1993; Abou-Dief and El-Akkad, 1999; Bacha and Bacha, 2012; Hamdi et al., 2013) The population of villi was greatest in the jejunum, followed by the ileum and least in the duodenum The villi of the mucosa of all segments of the African pied crow presumably increased the surface area for contact with the digesta thereby increasing the efficiency of breaking down and absorption of the nutrients This is because the small intestine is known to be the primary site of absorption of most nutrients taken orally in both mammals and birds (Isshiki et al., 1989; Lavin et al., 2008) However, from the results of the present study, the villi characteristics are not in agreement with earlier findings in chicken where a proximo-distal decreasing gradient from the duodenum to the ileum was reported (Denbow, 2000; Yasar and Forbes, 1999) Tallest villi were found in the jejunum followed by the duodenum and least at the ileum Longer villi suggest increased epithelial progenitor 58 Table C.G Okpe et al Gross and Histometric data of components of the small intestine Length of segments (cm) ± SEM Weight of segments (g) ± SEM Relative organ body weight of intestinal segments% ± SEM Weight: length ratio of intestinal segments Mean number of villi ± SEM Mean height of villi (lm) ± SEM Mean width of villi (lm) ± SEM Area of villus (lm2) Mean depth of crypt (lm) ± SEM Villus height: crypt depth ratio ± SEM Mean number of goblet cells per villus per segment ± SEM Width of tunica muscularis per segment (lm) ± SEM Different superscripts abcd Duodenum Jejunum Ileum 20.47 ± 0.25a 5.89 ± 0.17a 0.01 ± 0.0000a 0.39 ± 0.008a 43.33 ± 1.36a 7.37 ± 0.21a 0.70 ± 0.02a 5.15 ± 0.19a 1.03 ± 0.05a 7.41 ± 0.35a 80.80 ± 1.47a 0.84 ± 0.05a 28.32 ± 0.26b 7.92 ± 0.19b 0.02 ± 0.00013b 0.21 ± 0.007b 64.20 ± 2.16b 16.38 ± 0.75b 0.82 ± 0.04b 13.22 ± 0.70b 0.94 ± 0.04a 17.56 ± 0.74b 88.07 ± 1.84b 2.27 ± 0.10b 19.12 ± 0.23c 1.43 ± 0.10c 0.01 ± 0.0000a 0.08 ± 0.003c 49.2 ± 1.70c 6.21 ± 0.37c 0.89 ± 0.04c 5.68 ± 0.57a 2.33 ± 0.12b 2.71 ± 0.14c 111.87 ± 3.73c 1.65 ± 0.13c in a column indicate significant difference (P 0.05) proliferation and decreased epithelial turnover (Erwin et al., 2006; Dekaney et al., 2007; Wang et al., 2007) The increased villi height in the jejunum may be an indication of greater cell proliferation in that segment The branching and anastomoses of the villi reported in the present study appears not to have been reported in any other breed of bird This anatomical modification probably increased the surface area for contact with the ingesta and thus more efficient absorption of nutrients In order to extract more nutrients with less gut mass and length, the villus amplification ratio has been reported to be greater in avian species compared with mammalian species (Lavin et al., 2008) The findings in the present study suggest that the greater proportion of absorption of nutrients takes place in the jejunum of the African pied crow This inference is based on earlier report which stated that the density and size of villi and microvilli of small intestine are directly related with the absorption capacity of the bird (Macari, 1995) Moreover, the surface area of the segments determines the area over which nutrient digestion and absorption takes place However the features of the villi observed in the present study differed from other observations where the length and number of villi in birds were reported to be greatest in the duodenum and decreases towards the ileum (Bacha and Bacha, 2012; Zaher et al., 2012; Hamdi et al., 2013) The variations may be due to differences in phylogenetic signals The distributions of goblet cells in this study were in a proximo-distal increasing gradient Similar distribution pattern has been described in other birds and mammals, producing secretions that contain mucopolysaccharides (Banks, 1993; Nasrin et al., 2012) The positive staining of the goblet cells of the villi and crypts to PAS and Alcian blue indicates the presence of both acid and neutral mucopolysaccharides within its contents This is in agreement with reports of El-Banhawy et al (1993) Goblet cells produce mucus, increased number of goblet cells in some of the segments suggests greater elaboration of mucus which probably enhances the movement of digesta and nutrient digestability Smirnov et al (2004) opined that mucus acts as a medium where absorption processes take place The mucin in the secretion may offer protection to the mucosal surface from chemical irritants, micro-organisms and abrasion from the digesta The mucus produced as well probably provided a smooth lubricated mucosal surface that facilitates transportation of the digesta This view is supported by reports that the mucous produced by goblet cells provide protective and transport roles in the intestines (Specian and Oliver, 1991; Montagne et al., 2004; Plaisancie, 2006) By the time intestinal contents reach the distal part of small intestine, most of the nutrients may have been absorbed, the digesta are rougher, moisture content relatively reduced This may be responsible for increased population of goblet cells seen in the ileum Also, the goblet cells secretions probably contribute to the energy requirement of the microvilli and epithelial cells Energy is needed in the breakdown and absorption of the intestinal content Mucins could provide such energy as they are glycoproteins consisting of 50% carbohydrate (Banks, 1993) The lamina priopria of all three segments of the small intestine of the African pied crow were laden with mucosal glands These glands probably secrete large amount of various digestive enzymes necessary for breakdown and absorption of the digesta Southgate (1995) reported that enzymes and nutrient transporters needed for the breakdown and absorption of nutrients are in greatest quantity within the small intestine The tunica muscularis in the walls of all the segments of small intestine of the African pied crow were similar to those of other birds and were most probably involved in the peristaltic activities that propel the intestinal content towards the large intestine (Banks, 1993; Aughey and Frye, 2001) However, the tunica muscularis of the jejunum was thicker than that of duodenum and ileum respectively From findings of longer jejunum, preponderance of villi, increased surface area of the villi, it is suggestive that greater percentage of digestion and absorption take place at the jejunum The thick muscular wall probably allows more mixing or mechanical digestion of feed and quickened propelling of digesta, thus minimizing digestive load This histological adaptation may enhance movement of the intestinal content through the spiral coils of the jejunum Tunica serosa is similar to that described for other birds (Bacha and Bacha, 2012) Conclusion The jejunum of African pied crow was modified into cone shaped spiral coils The villi were wavy in shape and formed anastomosing network All the morphometric parameters studied were comparatively higher in the jejunum These mor- Morphological adaptations of the small intestine of the African pied crow phological modifications most probably maximize space for improved absorption Conflict of interest The authors declare that there are no conflicts of interest regarding this study References Abou-Dief, F., El-Akkad, M., 1999 Histological and ultra structural studies on the ileum of the Cattle Egret, Egretta ibis ibis J Egypt Ger Soc Zool 30, 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Note the mucosal glands (MG) Alcian Blue stain Morphological adaptations of the small intestine of the African pied crow length, width, areas and population of villi in the three segments of the