Anatomia, Histologia, Embryologia
ORIGINAL ARTICLE
Anatomical Study of the Gastrointestinal Tract in Free-living Axis Deer (Axis axis) rez1*, S. Erdogan2 and R. Ungerfeld3 W. Pe blica, Lasplaces 1620, 11600 Montevideo, Uruguay; de Anatomıa, Facultad de Veterinaria, Universidad de la Repu Addresses of authors:1 Area Department of Anatomy, Faculty of Veterinary Medicine, University of Dicle, Diyarbakir 21280, Turkey; 3 blica, Lasplaces 1620, 11600 Montevideo, Uruguay Departamento de Fisiologıa, Facultad de Veterinaria, Universidad de la Repu 2
*Correspondence: Tel.: +598 2 6229575; fax: +598 2 6280130; e-mail: [email protected] With 5 figures Received April 2013; accepted for publication January 2014 doi: 10.1111/ahe.12106
Summary The macroscopic anatomy of the stomach and intestines of adult axis deer (Axis axis), a cervid species considered intermediate/mixed feeder, was observed and recorded. Nine adult wild axis deers of both sexes were used and studied by simple dissection. The ruminal papillae were distributed unevenly in the overall area of the inner surface of rumen and primarily were more large and abundant within the atrium. The ruminal pillars had no papillae. There was an additional ruminal pillar located between the right longitudinal and right coronary ventral pillars connected to the caudal pillar. No dorsal coronary pillars were found, and the ventral coronary pillars are connected. The reticulum was the third compartment in size, and the maximum height of the reticular crests was 1.0 mm. The Cellulae reticuli were not divided and rarely contained secondary crests. There were no Papillae unguiculiformes. The omasum was the smallest gastric compartment. The abomasum had about twelve spiral plicae, and a small pyloric torus was present. The intraruminal papillation was similar to those species that are characterized by a higher proportion of grass in their natural diet. The finding of the small reticular crests is typical for browser ruminants and was coincident with data reported for other deer. The comparative ratio of the small intestine to the large intestine was 1.69, in terms of length measurements in axis deer and appears below of the ‘browser range’. We concluded that the gastrointestinal system of axis deer reflected similar morphological characteristics of the both types of ruminants: browser and grazer, and we consider it as an intermediate feeder.
Introduction According to their feeding types, ruminants are classified into three groups: browsers, intermediate feeders and grazers (Hofmann and Stewart, 1972; Hofmann, 1973, 1989). These categories have been defined based on anatomical studies, mainly performed in African, European, and North American species. Browser ruminants predominantly eat woody and non-woody dicotyledonous forage, such as tree foliage, herbs or wild fruits (e.g. Alces alces and Giraffa camelopardalis). On the other hand, grazer ruminants feed mainly graminaceous plants (e.g. Syncerus cafer and Ovis aries). Intermediate feeders consume monocotyledonous forage – grasses – to a certain degree, © 2014 Blackwell Verlag GmbH Anat. Histol. Embryol. 44 (2015) 43–49
but depend greatly on seasonal variation in forage availability (e.g. Taurotragus oryx and Rupicapra rupicapra; Hofmann and Stewart, 1972; Hofmann, 1973, 1988, 1989) while grazers, such as cattle, consume mostly lower-quality grasses. Hofmann (1973, 1988, 1989) reported that there are morphological differences on the digestive tract of the three categories and hypothesized on the consequent physiological differences. The grazer group has a large rumen, an unpapillated dorsal rumen mucosa, unpapillated and strong rumen pillars, evident reticular crests with secondary and tertiary crests, and a comparatively large omasum with four orders of laminae. Typical characteristics of browser ruminants are ruminal papillae evenly distributed
43
W. Perez, S. Erdogan and R. Ungerfeld
Anatomy of Gastrointestinal Tract in Axis Deer
across the rumen, papillated rumen pillars, large reticulum with low reticular crests and a small omasum (Hofmann, 1973, 1988, 1989; Clauss et al., 2006; Clauss et al., 2009; Clauss et al., 2010). According to Hofmann (1989), the length ratio of the small intestine/ large intestine is 1.9–2.7 in browsers, and 4.0–4.5 in grazer ruminants. Most cervid species are considered either browsers or intermediate feeders, but until now none of them has been classified as grazer (Hofmann, 1985). Hofmann (1985) classified the axis deer, also known as chital deer, as an intermediate/mixed feeder. In the same direction, Rodgers (1988) had categorized it as a generalist feeder, with a diet consisting of grasses, forbs and leaves of woody plants. The percentage of grass in its natural diet is approximately 70% (Van Wieren, 1996). To the best of our knowledge, there is no information on the macroscopic anatomy of the gastrointestinal tract of the Axis axis. Therefore, we aimed to describe the anatomical characteristics of the axis stomach and based on its stomach anatomy discuss on its possible feeding strategies. Materials and Methods Nine animals were hunted by commissionable hunters of military from a free-living axis deer population, located at the ‘Estancia Presidencial Parque Anchorena’ (EPA), Colonia, Uruguay (34.3°S 58.0°W) to maintain the population control. The axis deer has been introduced in this place in the 1920s; now, there are more than 1000 individuals living free at the EPA and the surrounding areas, protected from hunting except for scientific purposes. Animals have free access to abundant native pastures, trees to browse and improved pastures and corn crop in the fields surrounding the EPA. The specimens were handled and treated according to the local Ethical Board guidelines of University of the Republic, Uruguay. Two adult females (49.0 kg) and seven adult males (66.4 6.4 kg) in excellent body condition were hunted and immediately dissected.
a
The ventral abdominal wall of each animal was dissected, and the stomach was removed after sectioning the oesophagus just prior to the diaphragm, and the pylorus just before the duodenum. Stomach contents were measured by weighing the unopened organ and reweighing it after it had been opened, and contents rinsed with tap water and dried with paper towels. Anatomical measurements were taken following standard procedures described by Hofmann (1969). Briefly, the ruminoreticulum was placed on its left side, and the height and length of the rumen and the reticulum, and the length of the Curvatura omasi were measured with soft measuring tape. After incision, and emptying the stomach compartments, the dimensions of the Ostia intraruminale, ruminoreticulare and reticuloomasale were measured with a tape. The thicknesses of the cranial and caudal rumen pillars and the maximum heights of the reticular crests were measured with callipers. For precise measurements of the curved structures, a flexible yarn was used firstly and then yarn was measured by calliper. The full and empty weights of stomach were also recorded. The intestinal tract was separated after sectioning the pylorus just prior to the duodenum and dissecting it away from its attachments to the dorsal abdominal wall. The descending colon was tied off just prior the entrance of the pelvic cavity. After removal of all mesenteric attachments, the lengths of the different sections of the intestinal tract on the anti-mesenteric side were taken with a standard measuring tape. Pictures were taken with a digital camera (Nikon D7000; Nikon Corporation, Tokyo, Japan). Terms are used in agreement with the Nomina Anatomica Veterinaria (2012). The results are presented as mean SD. Results The stomach of the axis deer was composed of the four classic compartments of the ruminants (Fig. 1). The weight of all the full stomach was 9.57 0.83 kg.
b
(iv)
(iii) (i) (ii)
44
Fig. 1. (a) Right side of the stomach. 1: dorsal sac of the rumen, 2: ventral sac of the rumen, 3: right longitudinal sulcus, 4: ventral coronary sulcus, 5: Saccus caecus caudoventralis, 6: reticulum, 7: omasum, 8: abomasum. (b) External projections of internal pillars on the right surface of the rumen. (i): additional pillar, (ii): right ventral coronary pillar, (iii): right accessory pillar, (iv): right longitudinal pillar. Scale: millimetre rule.
© 2014 Blackwell Verlag GmbH Anat. Histol. Embryol. 44 (2015) 43–49
W. P erez, S. Erdogan and R. Ungerfeld
The ruminoreticulum weighed 8.96 0.80 kg full and 1.342 0.13 kg empty (14.4 5.2% and 2.2 0.2% respect the body weight). The dorsal and ventral sacs of the rumen lengths were 43.9 2.6 cm and 37.8 2.1 cm, respectively. The height of the rumen measured 39.3 2.3 cm. The Saccus caecus caudoventralis was extended more caudally than the Saccus caecus caudodorsalis (Fig. 1a). The dorsal sac communicated with the ventral sac through the Ostium intraruminale, whose border was formed by the ruminal pillars and measured between 18 9 14 and 25 9 18 cm. The cranial and caudal ruminal pillars were the most evident and thickest pillars of the ruminal mucosa, and the thicknesses of the cranial and caudal ruminal pillars measured 8.1 0.7 mm and 13.0 1.7 mm, respectively. In both lateral sides of the rumen, the right and left ends of the cranial pillar extended caudally, as the longitudinal pillars. The left longitudinal pillar was shorter and did not reach the caudal pillar. The right end of the caudal pillar was divided into three branches: the continuation of the caudal pillar into the right longitudinal pillar, the ventral coronary pillar connected with the left ventral coronary pillar and one additional pillar. There was an additional ruminal pillar (Fig. 2) located between the longitudinal right and the right coronary ventral pillars, emerging in the caudal pillar. Although internal additional pillar was very visible, there was no evident groove that corresponds with the additional ruminal pillar on the external right surface of the rumen, but external projection of additional pillar was shown in Fig. 1B. The left end of the caudal pillar only gave the ventral coronary pillar connected with the right ventral coronary pillar. The left end of the caudal pillar does not connect with the left longitudinal pillar, and there was no left
Fig. 2. Interna1 view of the rumen. 1: caudal pillar, 2: right ventral coronary pillar, 3: additional pillar, 4: right longitudinal pillar, 5: right accessory pillar. Scale: millimetre rule.
© 2014 Blackwell Verlag GmbH Anat. Histol. Embryol. 44 (2015) 43–49
Anatomy of Gastrointestinal Tract in Axis Deer
accessory pillar. No dorsal coronary pillars were observed in any side of the caudal pillar. The facts of the ventral coronary pillars were connected on both sides leaving the caudoventral blind sac encircled completely by pillars. The Ostium ruminoreticulare measured between 8.0 9 8.0 and 11.0 9 11.0 cm. The ruminal papillae were distributed unevenly in the overall area of the inner surface of the rumen, were mostly larger and abundant in the atrium and were also present in the dorsal sac. The ruminal pillars had no papillae. The ruminal papillae gradually heightened and continued with the cristae reticuli cranial to the Plica ruminoreticularis. The reticulum was the third compartment in size (Fig. 1). Its height and craniocaudal length were 19.2 0.8 cm and 11.6 1.2 cm, respectively. The full and empty reticulum weighed 394 153 g, and 98.5 15.3 g, respectively. The maximum height of the reticular cristae was 1.0 mm (Fig. 3). The Cellulae reticuli, which has honeycomb appearance, were not divided and rarely contained secondary crests. They were broader and deeper near the greater curvature and become smaller towards the lesser curvature of the reticulum. There was no Papillae unguiculiformes at the reticulo-omasal orifice (Fig. 3), which diameter measured 23.8 1.8 mm. The omasum was the smallest gastric compartment. The height of omasum was 13.5 0.9 cm, while its craniocaudal length measured 10.4 1.0 cm, and the Curvatura omasi 28.5 1.8 cm. It weighed 310.0 42.8 g and 127.5 15.1 g full and empty, respectively. The sides of the Laminae omasi were marked by the presence of the Papillae omasi. The abomasum was the second compartment in size, and the curvature major and minor lengths were 41.9 1.8 cm
Fig. 3. Reticuloomasal orifice (*), R: reticulum, O: omasum. Scale: millimetre rule.
45
Anatomy of Gastrointestinal Tract in Axis Deer
and 20.9 1.4 cm, respectively. The full and empty abomasum weighed 307.5 24.2 g and 158.8 12.3 g, respectively. The abomasum had approximately 12 Plicae spirales abomasi and a small Torus pyloricus. The small intestine measured 1078 202 cm and was clearly divided into duodenum, jejunum and ileum. The cranial part of the duodenum was continued with a descending portion, situated in the dorsal part of the right flank. The right lobule of the pancreas, which was located within the mesoduodenum, adhered to the cranial portion of the descending duodenum. After a caudal flexure, the ascending part of the duodenum ran in parallel to the descending part and was accompanied by the first portion of the descending colon. The limit between duodenum and jejunum was marked by the duodenojejunal flexure. The ileum was the terminal part of the small intestine attached to the caecum by the ileocecal fold (Fig. 4) and was opened into the large intestine through the ileal ostium, which was found at the junction of the caecum with the ascending colon. The gross intestine was composed of caecum, ascending colon, transverse colon, descending colon, rectum and canal anal. The gross intestine length was 637 60 cm. The length ratio of the small intestine/large intestine was 1.69. The caecum length was 32.5 2.3 cm, and its full and empty weights were 430.0 31.4 g and 52.3 5.4 g. The caecum (Fig. 4) was attached to the ileum by a long ileocecal fold and to the proximal ansa of the ascending colon by a short cecocolic fold (Fig. 4). Both the caecum and the colon were smooth externally and did not have sacculations or bands. The ascending colon was the most developed portion of the whole intestine, and it had the most complex
Fig. 4. Right side view of the intestine. 1: caecum, 2: ileum, 3: ileocecal fold, 4: jejunum, 5: descending colon. Scale: millimetre rule.
46
W. Perez, S. Erdogan and R. Ungerfeld
arrangement. The ascending colon (Figs 4 and 5) had three ansae: the proximal ansa, the spiral ansa and the distal ansa. The caecum and the proximal ansa were the widest portion of the intestine. The proximal ansa of the ascending colon was S-shaped, directed first cranially, turned over itself caudally, adhering to the cranial part of the caecum and finally turned medially where it attached to the left sheet of mesentery. The length of the proximal ansa was 44.8 6.8 cm, and its full and empty weights were 360 58 g and 65 7 g, respectively. The spiral ansa was formed by 2.5 centripetal gyri, a central flexure and 2.5 centrifugal gyri (Fig. 5). The last centrifugal gyrus left the spiral and ran near the jejunum. This last part, once it reached the root of the mesentery, was placed within the concavity of the proximal ansa, where it became the distal ansa of the ascending colon (Fig. 5) and continued cranially by the transverse colon, at the level of the right colic flexure. At the level of the left colic flexure, the transverse colon was followed by the descending colon. The latter continued as rectum at the entrance of the pelvic cavity. The intestinal tract was mainly situated on the right side and was included in its majority within the supraomentalis recess. The greater omentum covered almost all the right side and almost all the intestine, with the exception of the descending duodenum. The superficial wall of the great omentum originated from the left longitudinal sulcus of the rumen, and the deep wall in the right longitudinal sulcus. Dorsally and to the right, the superficial wall was attached to the descending duodenum, and the deep wall was attached more ventrally, to the distal ansa of the ascending colon.
Fig. 5. Left side view of the intestine. 1: caecum, 2: ileum, 3: ansa proximalis coli, 4: ansa spiralis coli, 5: last centrifugal gyrus of ansa spiralis coli, 6: ansa distalis coli, 7: jejunum. Scale: millimetre rule.
© 2014 Blackwell Verlag GmbH Anat. Histol. Embryol. 44 (2015) 43–49
W. P erez, S. Erdogan and R. Ungerfeld
There were no sex-related differences in the anatomical characteristics and topographical structure of the gastrointestinal tract. Discussion To the best of our knowledge, this is the first anatomical description of the gastrointestinal tract of the axis deer. To fully understand the functional mechanisms of the gastrointestinal tract, firstly, anatomical characteristics of the gastrointestinal system have to be fully understood. In this sense, Hofmann (1989) hypothesized that ruminant diversity in the structure of the gastrointestinal tract (and some other structures) represents adaptations to the diversity of diets. Knowledge of differential characteristics of the digestive morphology would improve our understanding of their feeding habits and diets and clarify the classification systems (Steinheim et al., 2003). Overall, according to the anatomical characteristics of the gastrointestinal anatomy, and in agreement with previous reports (Hofmann, 1985; Rodgers, 1988), the axis deer may be considered an intermediate feeder. In our studied animals, the ruminal papillae were distributed unevenly in the rumen and were more large and abundant within the atrium. The development of these papillae is stimulated by the presence of volatile fatty acids (VFA; Warner et al., 1956; Sander et al., 1959; Sakata and Tamate, 1978, 1979). Because VFA production depends in part of diet quality, the number and size of ruminal papillae reflect variation in diet quality, for example, within a species between seasons (Hofmann, 1973; K€ onig et al., 1976; Hofmann and Nygren, 1992; Josefsen et al., 1996; Forsyth and Fraser, 1999) or between free-living and captive individuals (Hofmann and Matern, 1988; Hofmann and Nygren, 1992; Lentle et al., 1996). In our template climate, grass is available in all seasons; we think that there are no differences between foods in all months of the year, but we need more studies for confirmation. The papillation of the rumen can be indicative for stratification, with even papillation indicating homogenous contents and uneven papillation stratified contents (Clauss et al., 2009). The surface enlargement factor of axis deer according to Clauss et al. (2009) was 1.5, 1.9 and 7.0 for the dorsal sac, ventral sac and atrium of the rumen, respectively. The observed differences in the intraruminal papillation pattern correspond to species characterized by a high proportion of grass in their natural diet (Clauss et al., 2009). The fact that we could observe evident differences in the papillation between the dorsal rumen and the atrium ruminis indicates that the ruminoreticulum physiology of the axis deer is not similar to ‘moose-type’ ruminants, which have an homogenous intraruminal papillation (Clauss et al., 2009) and © 2014 Blackwell Verlag GmbH Anat. Histol. Embryol. 44 (2015) 43–49
Anatomy of Gastrointestinal Tract in Axis Deer
homogenous/unstratified ruminoreticulum contents (Clauss et al., 2010). Thus, the papillation pattern of the ruminoreticulum (and therefore ruminoreticulum contents stratification) fits into that described in deer adapted to a high proportion of monocot material in the natural diet (Clauss et al., 2009), typical for many mixed feeder and grazing species. In the axis deer, the ruminal papillae were mostly larger and abundant in the atrium and the dorsal sac. Clauss et al. (2009) mentioned the surface enlargement factor of the rumen papillae in the different parts of the rumen and compare it with other ruminant species. The high number and larger size of papillae in the lower part of the atrium ruminis was expected as this is the main absorptive area in all ruminant species (Kay et al., 1980; Hofmann, 1989). Similarly, the highest papillae density mostly occurred in the atrium ruminis for sika deer (Fraser, 1996). On the other hand, the highest density of ruminal papilla was determined in the ventral sac of rumen for red deer (Fraser, 1996). In sika deer, papillae on the dorsal rumen wall were generally short and tapered (Fraser, 1996). The existence of an additional pillar between the longitudinal right and the right coronary ventral pillars in the right side of the rumen was an unexpected finding. According to our knowledge, a similar additional pillar was only reported in the Egyptian water buffalo (Hemmoda and Berg, 1980), but it does not exist in the domestic ruminants. There were no dorsal coronary pillars, and the ventral coronary pillars were connected. Barone (1997) mentioned that dorsal coronary pillars are absent in the ewe and that the ventral coronary pillars fail to join in the domestic ruminants. This disposition of pillars may be indicative of a different mechanism of the rumen contraction. However, we could not find study on rumen contraction on any deer species. Neural regulation of the motility is crucial for the regulation and coordination of the regional specific motility of the rumen and their pillars (Pfannkuche et al., 2002). M€ unnich et al. (2008) suggested that the rumen of grazers is under a stronger excitatory control than the rumen of intermediate-type species. The functional significance of our findings of an additional pillar and their nervous control should be analysed in further studies. The existence of the small reticular crests agrees with data used by Clauss et al. (2010) for other deer and with what we observed in the pampas deer (Perez and Ungerfeld, 2012). Teixeira et al. (2009) suggest that the unguiculiform papillae may act as a filter barrier to selectively keep back those particles of inappropriate size not suitable to be forwarded into the omasum and abomasum. The absence of these papillae in our studied axis deer can implicate that this species have a different flow of the stomach contents
47
W. Perez, S. Erdogan and R. Ungerfeld
Anatomy of Gastrointestinal Tract in Axis Deer
and more fluid contents in this area; according to Hofmann (1989) the reticular groove can function in browsers as observed in suckling young ruminants, but this is a hypothetical mechanism that needs more research. As the ruminants with a high proportion of grass in their natural diet have large omasa (Hofmann, 1973, 1988, 1989; Clauss et al., 2006), the smaller omasum compared with the reticulum reaffirms the possibility of considering the axis deer as an intermediate feeder. Among the Cervidae, a large heavy omasum as in cattle was recorded only in Elaphurus davidianus (Hofmann, 1985). A limitation of this study is that we did not determine the omasal lamina size, so we cannot compare it with that of other species. The abomasum was similar to that observed in domestic ruminants (Barone, 1997). The small intestine of the axis deer was similar to that of the domestic ruminants (Barone, 1997). As in bovines, ovines and caprine (Barone, 1997), pampas deer (Perez et al., 2008), giraffe (Perez et al., 2009) and brown brocket deer (Perez and Vazquez, 2012), the ascending colon had three ansae (proximal, spiral and distal). Also in agreement with the literature of the domestic ruminants, the spiral ansa consisted of centripetal gyri, a central flexure and centrifugal gyri (Barone, 1997; Nomina Anatomica Veterinaria, 2012). The small/large intestine ratio (1.69) is less than the 1.9–2.7 ratio of the browsers (Hofmann, 1989). The ratio of 1.3–2.0 in the strictly browser species as giraffe and okapi (Perez et al., 2009) is even below this range. Brown brocket deer, other browser deer, have a ratio of 2.0 (Perez and Vazquez, 2012). In contrast, grazers as the domestic cattle achieve ratios of 4.0–5.5, even greater than the range of 4.0–5.0 given by Hofmann (1989) for typical grazers. However, long large intestines have also been observed in several grazing wild ruminant species (Hofmann, 1999; Clauss et al., 2005; Perez et al., 2008). Therefore, it seems that rather than characterizing a difference between feeding types, the observed differences in intestinal ratios more likely set cattle-like ruminants apart from other ruminant species. The anatomy of the gastrointestinal tract of axis deer agrees with reports on its natural feeding habits (Rodgers, 1988; Van Wieren, 1996) and with the classification of Hofmann (1985) as an intermediate feeder. Its morphology of intermediate-type deer allowed to consume a wide range of vegetable diets that emphasize the evolutionary flexibility of the ruminant digestive system. Acknowledgements Authors acknowledge to Divisi on de Fauna from the Ministerio de Ganaderıa, Agricultura y Pesca, and to Parque Anchorena of the Presidencia de la Rep ublica.
48
References Barone, R., 1997: Anatomie comparee des mammiferes domestiques. Tome 3, Edit. 3 (Splanchnologie I. Appareil digestif, appareil respiratoire). Paris: Vigot Freres. Clauss, M., J. Hummel, F. Vercammen, and W. J. Streich, 2005: Observations on the macroscopic digestive anatomy of the Himalayan Tahr (Hemitragus jemlahicus). Anat. Histol. Embryol. 34, 276–278. Clauss, M., R. R. Hofmann, J. Hummel, J. Adamczewski, K. Nygren, C. Pitra, and S. Reese, 2006: The macroscopic anatomy of the omasum of free-ranging moose (Alces alces) and muskoxen (Ovibos moschatus) and a comparison of the omasal laminal surface area in 34 ruminant species. J. Zool. 270, 346–358. Clauss, M., R. R. Hofmann, J. Fickel, W. J. Streich, J. Hummel, and G. W. Foundation, 2009: The intraruminal papillation gradient in wild ruminants of different feeding types: implications for rumen physiology. J. Morphol. 270, 929–942. Clauss, M., R. R. Hofmann, W. J. Streich, J. Fickel, and J. Hummel, 2010: Convergence in the macroscopic anatomy of the reticulum in wild ruminant species of different feeding types and a new resulting hypothesis on reticular function. J. Zool. 281, 12–25. Forsyth, D. M., and K. W. Fraser, 1999: Seasonal changes in the rumen morphology of Himalayan tahr (Hemitragus jemlahicus) in the two thumb range. South Island, New Zealand. J. Zool. 249, 241–248. Fraser, K. W., 1996: Comparative rumen morphology of sympatric sika deer (Cervus nippon) and red deer (C. elaphus scoticus) in the Ahimanawa and Kaweka Ranges, central North Island, New Zealand. Oecologia. 105, 160–166. Hemmoda, A. S. K., and R. Berg, 1980: Gross-anatomical Studies on the Ruminal Pillar System of the Egyptian Water Buffalo (Bos bubalis L.). Anat. Histol. Embryol. 2, 148–154. Hofmann, R. R., 1969: Zur Topographie und Morphologie des Wiederk€auermagens im Hinblick auf seine Funktion (nach vergleichenden Untersuchungen an Material ostafrikanischer Wildarten). J. Vet. Med. Suppl. 10, 1–180. Hofmann, R. R., 1973: The Ruminant Stomach. Nairobi: East African Literature Bureau. Hofmann, R. R., 1985: Digestive physiology of the deer – their morphophysiological specialisation and adaptation. R. Soc. N. Z. Bull. 22, 393–407. Hofmann, R. R., 1988: Morphophysiological evolutionary adaptations of the ruminant digestive system. In: Aspects of Digestive Physiology in Ruminants. (A. Dobson and M. Dobson, eds). Ithaca, NY: Cornell University Press. pp. 1–20. Hofmann, R. R., 1989: Evolutionary steps of ecophysiological adaptation and diversification of ruminants: a comparative view of their digestive system. Oecologia. 78, 443–457. Hofmann, R. R., 1999: Functional and comparative digestive system anatomy of Arctic ungulates. Rangifer. 20, 71–81.
© 2014 Blackwell Verlag GmbH Anat. Histol. Embryol. 44 (2015) 43–49
W. P erez, S. Erdogan and R. Ungerfeld
Hofmann, R. R., and B. Matern, 1988: Changes in gastrointestinal morphology related to nutrition in giraffes (Giraffa camelopardalis): a comparison of wild and zoo specimens. Int. Zoo. Yb. 27, 168–176. Hofmann, R. R., and K. Nygren, 1992: Ruminal mucosa as indicator of nutritional status in wild and captive moose. Alces Suppl. 1, 77–83. Hofmann, R. R., and D. R. M. Stewart, 1972: Grazers and browsers: a classification based on the stomach structure and feeding habits of East African ruminants. Mammalia. 36, 226–240. Josefsen, T. D., T. H. Aagnes, and S. D. Mathiesen, 1996: Influence of diet on the morphology of the ruminal papillae in reindeer calves (Rangifer tarandus). Rangifer. 16, 119–128. Kay, R. N. B., W. V. Engelhardt, and R. G. White, 1980: The digestive physiology of wild ruminants. In: Digestive Physiology and Metabolism in Ruminants. (Y. Ruckebusch and P. Thivend, eds). Lancaster: MTP Press. pp. 743–762. K€ onig, R., R. R. Hofmann, and G. Geiger, 1976: Differentiellmorphologische Untersuchungen der resorbierenden schleimhautoberfla che des pansens beim rehwild (Capreolus capreolus) im sommer und winter. Eur. J. Wildl. Res. 22, 191–196. Lentle, R. G., I. M. Henderson, and K. J. Stafford, 1996: A multivariate analysis of rumen papillary size in red deer (Cervus elaphus). Can. J. Zool. 74, 2089–2094. M€ unnich, J., G. G€abel, and H. Pfannkuche, 2008: Intrinsic ruminal innervation in ruminants of different feeding types. J. Anat. 213, 442–451. Nomina Anatomica Veterinaria, 2012: International Committee on Veterinary Gross Anatomical Nomenclature (I.C.V.G.A.N.), 5th edn revised. Hannover, Germany: Nomina Anatomica Veterinaria. Perez, W., and R. Ungerfeld, 2012: Gross anatomy of the stomach of the pampas deer, Ozotoceros bezoarticus (Artiodactyla: Cervidae). Zoologia (Curitiba). 29, 337–342. Perez, W., and N. Vazquez, 2012: Gross anatomy of the gastrointestinal tract in the Brown Brocket deer (Mazama gouazoubira). J. Morphol. Sci. 29, 148–150. Perez, W., M. Clauss, and R. Ungerfeld, 2008: Observations on the macroscopic anatomy of the intestinal tract and its
© 2014 Blackwell Verlag GmbH Anat. Histol. Embryol. 44 (2015) 43–49
Anatomy of Gastrointestinal Tract in Axis Deer
mesenteric folds in the pampas deer (Ozotoceros bezoarticus). Anat. Histol. Embryol. 37, 317–321. Perez, W., M. Lima, and M. Clauss, 2009: Gross anatomy of the intestine in the giraffe (Giraffa camelopardalis). Anat. Histol. Embryol. 38, 432–435. Pfannkuche, H., M. Schemann, and G. G€abel, 2002: Ruminal muscle of sheep is innervated by non-polarized pathways of cholinergic and nitrergic myenteric neurones. Cell Tissue Res. 309, 347–354. Rodgers, W. A., 1988: The wild grazing ungulates of India: an ecological review. In: Rangelands—Resource and Management. (P. Singh and P. S. Pathak, eds). Proceedings of the National Rangeland Symposium. Jhansi: IGFRI. pp. 404–419. Sakata, T., and H. Tamate, 1978: Rumen epithelial cell proliferation accelerated by rapid increase in intraruminal butyrate. J. Dairy Sci. 61, 1109–1113. Sakata, T., and H. Tamate, 1979: Rumen epithelial cell proliferation accelerated by propionate and acetate. J. Dairy Sci. 62, 49–52. Sander, E. G., R. G. Warner, H. N. Harrison, and J. K. Loosli, 1959: The stimulatory effect of sodium butyrate and sodium propionate on the development of the rumen mucosa in the young calf. J. Dairy Sci. 42, 1600–1605. Steinheim, G., L. A. Nordheim, R. B. Weladji, Ø. Holand, and T. Adnøy, 2003: Digestive tract anatomy of Norwegian sheep: difference between breeds. Acta Agric. Scand. A Anim. Sci. 3, 155–158. Teixeira, A. F., W. K€ uhnel, P. Vives, and T. Wedel, 2009: Functional morphology of unguiculiform papillae of the reticular groove in the ruminant stomach. Ann. Anat. 191, 469–476. Van Wieren, S. E., 1996: Browsers and grazers: foraging strategies in ruminants. In: Digestive Strategies in Ruminants and Nonruminants: Thesis Landbouw. (S. E. Van Wieren, ed.). Wageningen, The Netherlands: University of Wageningen. Warner, R. G., W. P. Flatt, and J. K. Loosli, 1956: Dietary factors influencing the development of the ruminant stomach. J. Agric. Food. Chem. 4, 788–792.
49
ORIGINAL ARTICLE
Anatomical Study of the Gastrointestinal Tract in Free-living Axis Deer (Axis axis) rez1*, S. Erdogan2 and R. Ungerfeld3 W. Pe blica, Lasplaces 1620, 11600 Montevideo, Uruguay; de Anatomıa, Facultad de Veterinaria, Universidad de la Repu Addresses of authors:1 Area Department of Anatomy, Faculty of Veterinary Medicine, University of Dicle, Diyarbakir 21280, Turkey; 3 blica, Lasplaces 1620, 11600 Montevideo, Uruguay Departamento de Fisiologıa, Facultad de Veterinaria, Universidad de la Repu 2
*Correspondence: Tel.: +598 2 6229575; fax: +598 2 6280130; e-mail: [email protected] With 5 figures Received April 2013; accepted for publication January 2014 doi: 10.1111/ahe.12106
Summary The macroscopic anatomy of the stomach and intestines of adult axis deer (Axis axis), a cervid species considered intermediate/mixed feeder, was observed and recorded. Nine adult wild axis deers of both sexes were used and studied by simple dissection. The ruminal papillae were distributed unevenly in the overall area of the inner surface of rumen and primarily were more large and abundant within the atrium. The ruminal pillars had no papillae. There was an additional ruminal pillar located between the right longitudinal and right coronary ventral pillars connected to the caudal pillar. No dorsal coronary pillars were found, and the ventral coronary pillars are connected. The reticulum was the third compartment in size, and the maximum height of the reticular crests was 1.0 mm. The Cellulae reticuli were not divided and rarely contained secondary crests. There were no Papillae unguiculiformes. The omasum was the smallest gastric compartment. The abomasum had about twelve spiral plicae, and a small pyloric torus was present. The intraruminal papillation was similar to those species that are characterized by a higher proportion of grass in their natural diet. The finding of the small reticular crests is typical for browser ruminants and was coincident with data reported for other deer. The comparative ratio of the small intestine to the large intestine was 1.69, in terms of length measurements in axis deer and appears below of the ‘browser range’. We concluded that the gastrointestinal system of axis deer reflected similar morphological characteristics of the both types of ruminants: browser and grazer, and we consider it as an intermediate feeder.
Introduction According to their feeding types, ruminants are classified into three groups: browsers, intermediate feeders and grazers (Hofmann and Stewart, 1972; Hofmann, 1973, 1989). These categories have been defined based on anatomical studies, mainly performed in African, European, and North American species. Browser ruminants predominantly eat woody and non-woody dicotyledonous forage, such as tree foliage, herbs or wild fruits (e.g. Alces alces and Giraffa camelopardalis). On the other hand, grazer ruminants feed mainly graminaceous plants (e.g. Syncerus cafer and Ovis aries). Intermediate feeders consume monocotyledonous forage – grasses – to a certain degree, © 2014 Blackwell Verlag GmbH Anat. Histol. Embryol. 44 (2015) 43–49
but depend greatly on seasonal variation in forage availability (e.g. Taurotragus oryx and Rupicapra rupicapra; Hofmann and Stewart, 1972; Hofmann, 1973, 1988, 1989) while grazers, such as cattle, consume mostly lower-quality grasses. Hofmann (1973, 1988, 1989) reported that there are morphological differences on the digestive tract of the three categories and hypothesized on the consequent physiological differences. The grazer group has a large rumen, an unpapillated dorsal rumen mucosa, unpapillated and strong rumen pillars, evident reticular crests with secondary and tertiary crests, and a comparatively large omasum with four orders of laminae. Typical characteristics of browser ruminants are ruminal papillae evenly distributed
43
W. Perez, S. Erdogan and R. Ungerfeld
Anatomy of Gastrointestinal Tract in Axis Deer
across the rumen, papillated rumen pillars, large reticulum with low reticular crests and a small omasum (Hofmann, 1973, 1988, 1989; Clauss et al., 2006; Clauss et al., 2009; Clauss et al., 2010). According to Hofmann (1989), the length ratio of the small intestine/ large intestine is 1.9–2.7 in browsers, and 4.0–4.5 in grazer ruminants. Most cervid species are considered either browsers or intermediate feeders, but until now none of them has been classified as grazer (Hofmann, 1985). Hofmann (1985) classified the axis deer, also known as chital deer, as an intermediate/mixed feeder. In the same direction, Rodgers (1988) had categorized it as a generalist feeder, with a diet consisting of grasses, forbs and leaves of woody plants. The percentage of grass in its natural diet is approximately 70% (Van Wieren, 1996). To the best of our knowledge, there is no information on the macroscopic anatomy of the gastrointestinal tract of the Axis axis. Therefore, we aimed to describe the anatomical characteristics of the axis stomach and based on its stomach anatomy discuss on its possible feeding strategies. Materials and Methods Nine animals were hunted by commissionable hunters of military from a free-living axis deer population, located at the ‘Estancia Presidencial Parque Anchorena’ (EPA), Colonia, Uruguay (34.3°S 58.0°W) to maintain the population control. The axis deer has been introduced in this place in the 1920s; now, there are more than 1000 individuals living free at the EPA and the surrounding areas, protected from hunting except for scientific purposes. Animals have free access to abundant native pastures, trees to browse and improved pastures and corn crop in the fields surrounding the EPA. The specimens were handled and treated according to the local Ethical Board guidelines of University of the Republic, Uruguay. Two adult females (49.0 kg) and seven adult males (66.4 6.4 kg) in excellent body condition were hunted and immediately dissected.
a
The ventral abdominal wall of each animal was dissected, and the stomach was removed after sectioning the oesophagus just prior to the diaphragm, and the pylorus just before the duodenum. Stomach contents were measured by weighing the unopened organ and reweighing it after it had been opened, and contents rinsed with tap water and dried with paper towels. Anatomical measurements were taken following standard procedures described by Hofmann (1969). Briefly, the ruminoreticulum was placed on its left side, and the height and length of the rumen and the reticulum, and the length of the Curvatura omasi were measured with soft measuring tape. After incision, and emptying the stomach compartments, the dimensions of the Ostia intraruminale, ruminoreticulare and reticuloomasale were measured with a tape. The thicknesses of the cranial and caudal rumen pillars and the maximum heights of the reticular crests were measured with callipers. For precise measurements of the curved structures, a flexible yarn was used firstly and then yarn was measured by calliper. The full and empty weights of stomach were also recorded. The intestinal tract was separated after sectioning the pylorus just prior to the duodenum and dissecting it away from its attachments to the dorsal abdominal wall. The descending colon was tied off just prior the entrance of the pelvic cavity. After removal of all mesenteric attachments, the lengths of the different sections of the intestinal tract on the anti-mesenteric side were taken with a standard measuring tape. Pictures were taken with a digital camera (Nikon D7000; Nikon Corporation, Tokyo, Japan). Terms are used in agreement with the Nomina Anatomica Veterinaria (2012). The results are presented as mean SD. Results The stomach of the axis deer was composed of the four classic compartments of the ruminants (Fig. 1). The weight of all the full stomach was 9.57 0.83 kg.
b
(iv)
(iii) (i) (ii)
44
Fig. 1. (a) Right side of the stomach. 1: dorsal sac of the rumen, 2: ventral sac of the rumen, 3: right longitudinal sulcus, 4: ventral coronary sulcus, 5: Saccus caecus caudoventralis, 6: reticulum, 7: omasum, 8: abomasum. (b) External projections of internal pillars on the right surface of the rumen. (i): additional pillar, (ii): right ventral coronary pillar, (iii): right accessory pillar, (iv): right longitudinal pillar. Scale: millimetre rule.
© 2014 Blackwell Verlag GmbH Anat. Histol. Embryol. 44 (2015) 43–49
W. P erez, S. Erdogan and R. Ungerfeld
The ruminoreticulum weighed 8.96 0.80 kg full and 1.342 0.13 kg empty (14.4 5.2% and 2.2 0.2% respect the body weight). The dorsal and ventral sacs of the rumen lengths were 43.9 2.6 cm and 37.8 2.1 cm, respectively. The height of the rumen measured 39.3 2.3 cm. The Saccus caecus caudoventralis was extended more caudally than the Saccus caecus caudodorsalis (Fig. 1a). The dorsal sac communicated with the ventral sac through the Ostium intraruminale, whose border was formed by the ruminal pillars and measured between 18 9 14 and 25 9 18 cm. The cranial and caudal ruminal pillars were the most evident and thickest pillars of the ruminal mucosa, and the thicknesses of the cranial and caudal ruminal pillars measured 8.1 0.7 mm and 13.0 1.7 mm, respectively. In both lateral sides of the rumen, the right and left ends of the cranial pillar extended caudally, as the longitudinal pillars. The left longitudinal pillar was shorter and did not reach the caudal pillar. The right end of the caudal pillar was divided into three branches: the continuation of the caudal pillar into the right longitudinal pillar, the ventral coronary pillar connected with the left ventral coronary pillar and one additional pillar. There was an additional ruminal pillar (Fig. 2) located between the longitudinal right and the right coronary ventral pillars, emerging in the caudal pillar. Although internal additional pillar was very visible, there was no evident groove that corresponds with the additional ruminal pillar on the external right surface of the rumen, but external projection of additional pillar was shown in Fig. 1B. The left end of the caudal pillar only gave the ventral coronary pillar connected with the right ventral coronary pillar. The left end of the caudal pillar does not connect with the left longitudinal pillar, and there was no left
Fig. 2. Interna1 view of the rumen. 1: caudal pillar, 2: right ventral coronary pillar, 3: additional pillar, 4: right longitudinal pillar, 5: right accessory pillar. Scale: millimetre rule.
© 2014 Blackwell Verlag GmbH Anat. Histol. Embryol. 44 (2015) 43–49
Anatomy of Gastrointestinal Tract in Axis Deer
accessory pillar. No dorsal coronary pillars were observed in any side of the caudal pillar. The facts of the ventral coronary pillars were connected on both sides leaving the caudoventral blind sac encircled completely by pillars. The Ostium ruminoreticulare measured between 8.0 9 8.0 and 11.0 9 11.0 cm. The ruminal papillae were distributed unevenly in the overall area of the inner surface of the rumen, were mostly larger and abundant in the atrium and were also present in the dorsal sac. The ruminal pillars had no papillae. The ruminal papillae gradually heightened and continued with the cristae reticuli cranial to the Plica ruminoreticularis. The reticulum was the third compartment in size (Fig. 1). Its height and craniocaudal length were 19.2 0.8 cm and 11.6 1.2 cm, respectively. The full and empty reticulum weighed 394 153 g, and 98.5 15.3 g, respectively. The maximum height of the reticular cristae was 1.0 mm (Fig. 3). The Cellulae reticuli, which has honeycomb appearance, were not divided and rarely contained secondary crests. They were broader and deeper near the greater curvature and become smaller towards the lesser curvature of the reticulum. There was no Papillae unguiculiformes at the reticulo-omasal orifice (Fig. 3), which diameter measured 23.8 1.8 mm. The omasum was the smallest gastric compartment. The height of omasum was 13.5 0.9 cm, while its craniocaudal length measured 10.4 1.0 cm, and the Curvatura omasi 28.5 1.8 cm. It weighed 310.0 42.8 g and 127.5 15.1 g full and empty, respectively. The sides of the Laminae omasi were marked by the presence of the Papillae omasi. The abomasum was the second compartment in size, and the curvature major and minor lengths were 41.9 1.8 cm
Fig. 3. Reticuloomasal orifice (*), R: reticulum, O: omasum. Scale: millimetre rule.
45
Anatomy of Gastrointestinal Tract in Axis Deer
and 20.9 1.4 cm, respectively. The full and empty abomasum weighed 307.5 24.2 g and 158.8 12.3 g, respectively. The abomasum had approximately 12 Plicae spirales abomasi and a small Torus pyloricus. The small intestine measured 1078 202 cm and was clearly divided into duodenum, jejunum and ileum. The cranial part of the duodenum was continued with a descending portion, situated in the dorsal part of the right flank. The right lobule of the pancreas, which was located within the mesoduodenum, adhered to the cranial portion of the descending duodenum. After a caudal flexure, the ascending part of the duodenum ran in parallel to the descending part and was accompanied by the first portion of the descending colon. The limit between duodenum and jejunum was marked by the duodenojejunal flexure. The ileum was the terminal part of the small intestine attached to the caecum by the ileocecal fold (Fig. 4) and was opened into the large intestine through the ileal ostium, which was found at the junction of the caecum with the ascending colon. The gross intestine was composed of caecum, ascending colon, transverse colon, descending colon, rectum and canal anal. The gross intestine length was 637 60 cm. The length ratio of the small intestine/large intestine was 1.69. The caecum length was 32.5 2.3 cm, and its full and empty weights were 430.0 31.4 g and 52.3 5.4 g. The caecum (Fig. 4) was attached to the ileum by a long ileocecal fold and to the proximal ansa of the ascending colon by a short cecocolic fold (Fig. 4). Both the caecum and the colon were smooth externally and did not have sacculations or bands. The ascending colon was the most developed portion of the whole intestine, and it had the most complex
Fig. 4. Right side view of the intestine. 1: caecum, 2: ileum, 3: ileocecal fold, 4: jejunum, 5: descending colon. Scale: millimetre rule.
46
W. Perez, S. Erdogan and R. Ungerfeld
arrangement. The ascending colon (Figs 4 and 5) had three ansae: the proximal ansa, the spiral ansa and the distal ansa. The caecum and the proximal ansa were the widest portion of the intestine. The proximal ansa of the ascending colon was S-shaped, directed first cranially, turned over itself caudally, adhering to the cranial part of the caecum and finally turned medially where it attached to the left sheet of mesentery. The length of the proximal ansa was 44.8 6.8 cm, and its full and empty weights were 360 58 g and 65 7 g, respectively. The spiral ansa was formed by 2.5 centripetal gyri, a central flexure and 2.5 centrifugal gyri (Fig. 5). The last centrifugal gyrus left the spiral and ran near the jejunum. This last part, once it reached the root of the mesentery, was placed within the concavity of the proximal ansa, where it became the distal ansa of the ascending colon (Fig. 5) and continued cranially by the transverse colon, at the level of the right colic flexure. At the level of the left colic flexure, the transverse colon was followed by the descending colon. The latter continued as rectum at the entrance of the pelvic cavity. The intestinal tract was mainly situated on the right side and was included in its majority within the supraomentalis recess. The greater omentum covered almost all the right side and almost all the intestine, with the exception of the descending duodenum. The superficial wall of the great omentum originated from the left longitudinal sulcus of the rumen, and the deep wall in the right longitudinal sulcus. Dorsally and to the right, the superficial wall was attached to the descending duodenum, and the deep wall was attached more ventrally, to the distal ansa of the ascending colon.
Fig. 5. Left side view of the intestine. 1: caecum, 2: ileum, 3: ansa proximalis coli, 4: ansa spiralis coli, 5: last centrifugal gyrus of ansa spiralis coli, 6: ansa distalis coli, 7: jejunum. Scale: millimetre rule.
© 2014 Blackwell Verlag GmbH Anat. Histol. Embryol. 44 (2015) 43–49
W. P erez, S. Erdogan and R. Ungerfeld
There were no sex-related differences in the anatomical characteristics and topographical structure of the gastrointestinal tract. Discussion To the best of our knowledge, this is the first anatomical description of the gastrointestinal tract of the axis deer. To fully understand the functional mechanisms of the gastrointestinal tract, firstly, anatomical characteristics of the gastrointestinal system have to be fully understood. In this sense, Hofmann (1989) hypothesized that ruminant diversity in the structure of the gastrointestinal tract (and some other structures) represents adaptations to the diversity of diets. Knowledge of differential characteristics of the digestive morphology would improve our understanding of their feeding habits and diets and clarify the classification systems (Steinheim et al., 2003). Overall, according to the anatomical characteristics of the gastrointestinal anatomy, and in agreement with previous reports (Hofmann, 1985; Rodgers, 1988), the axis deer may be considered an intermediate feeder. In our studied animals, the ruminal papillae were distributed unevenly in the rumen and were more large and abundant within the atrium. The development of these papillae is stimulated by the presence of volatile fatty acids (VFA; Warner et al., 1956; Sander et al., 1959; Sakata and Tamate, 1978, 1979). Because VFA production depends in part of diet quality, the number and size of ruminal papillae reflect variation in diet quality, for example, within a species between seasons (Hofmann, 1973; K€ onig et al., 1976; Hofmann and Nygren, 1992; Josefsen et al., 1996; Forsyth and Fraser, 1999) or between free-living and captive individuals (Hofmann and Matern, 1988; Hofmann and Nygren, 1992; Lentle et al., 1996). In our template climate, grass is available in all seasons; we think that there are no differences between foods in all months of the year, but we need more studies for confirmation. The papillation of the rumen can be indicative for stratification, with even papillation indicating homogenous contents and uneven papillation stratified contents (Clauss et al., 2009). The surface enlargement factor of axis deer according to Clauss et al. (2009) was 1.5, 1.9 and 7.0 for the dorsal sac, ventral sac and atrium of the rumen, respectively. The observed differences in the intraruminal papillation pattern correspond to species characterized by a high proportion of grass in their natural diet (Clauss et al., 2009). The fact that we could observe evident differences in the papillation between the dorsal rumen and the atrium ruminis indicates that the ruminoreticulum physiology of the axis deer is not similar to ‘moose-type’ ruminants, which have an homogenous intraruminal papillation (Clauss et al., 2009) and © 2014 Blackwell Verlag GmbH Anat. Histol. Embryol. 44 (2015) 43–49
Anatomy of Gastrointestinal Tract in Axis Deer
homogenous/unstratified ruminoreticulum contents (Clauss et al., 2010). Thus, the papillation pattern of the ruminoreticulum (and therefore ruminoreticulum contents stratification) fits into that described in deer adapted to a high proportion of monocot material in the natural diet (Clauss et al., 2009), typical for many mixed feeder and grazing species. In the axis deer, the ruminal papillae were mostly larger and abundant in the atrium and the dorsal sac. Clauss et al. (2009) mentioned the surface enlargement factor of the rumen papillae in the different parts of the rumen and compare it with other ruminant species. The high number and larger size of papillae in the lower part of the atrium ruminis was expected as this is the main absorptive area in all ruminant species (Kay et al., 1980; Hofmann, 1989). Similarly, the highest papillae density mostly occurred in the atrium ruminis for sika deer (Fraser, 1996). On the other hand, the highest density of ruminal papilla was determined in the ventral sac of rumen for red deer (Fraser, 1996). In sika deer, papillae on the dorsal rumen wall were generally short and tapered (Fraser, 1996). The existence of an additional pillar between the longitudinal right and the right coronary ventral pillars in the right side of the rumen was an unexpected finding. According to our knowledge, a similar additional pillar was only reported in the Egyptian water buffalo (Hemmoda and Berg, 1980), but it does not exist in the domestic ruminants. There were no dorsal coronary pillars, and the ventral coronary pillars were connected. Barone (1997) mentioned that dorsal coronary pillars are absent in the ewe and that the ventral coronary pillars fail to join in the domestic ruminants. This disposition of pillars may be indicative of a different mechanism of the rumen contraction. However, we could not find study on rumen contraction on any deer species. Neural regulation of the motility is crucial for the regulation and coordination of the regional specific motility of the rumen and their pillars (Pfannkuche et al., 2002). M€ unnich et al. (2008) suggested that the rumen of grazers is under a stronger excitatory control than the rumen of intermediate-type species. The functional significance of our findings of an additional pillar and their nervous control should be analysed in further studies. The existence of the small reticular crests agrees with data used by Clauss et al. (2010) for other deer and with what we observed in the pampas deer (Perez and Ungerfeld, 2012). Teixeira et al. (2009) suggest that the unguiculiform papillae may act as a filter barrier to selectively keep back those particles of inappropriate size not suitable to be forwarded into the omasum and abomasum. The absence of these papillae in our studied axis deer can implicate that this species have a different flow of the stomach contents
47
W. Perez, S. Erdogan and R. Ungerfeld
Anatomy of Gastrointestinal Tract in Axis Deer
and more fluid contents in this area; according to Hofmann (1989) the reticular groove can function in browsers as observed in suckling young ruminants, but this is a hypothetical mechanism that needs more research. As the ruminants with a high proportion of grass in their natural diet have large omasa (Hofmann, 1973, 1988, 1989; Clauss et al., 2006), the smaller omasum compared with the reticulum reaffirms the possibility of considering the axis deer as an intermediate feeder. Among the Cervidae, a large heavy omasum as in cattle was recorded only in Elaphurus davidianus (Hofmann, 1985). A limitation of this study is that we did not determine the omasal lamina size, so we cannot compare it with that of other species. The abomasum was similar to that observed in domestic ruminants (Barone, 1997). The small intestine of the axis deer was similar to that of the domestic ruminants (Barone, 1997). As in bovines, ovines and caprine (Barone, 1997), pampas deer (Perez et al., 2008), giraffe (Perez et al., 2009) and brown brocket deer (Perez and Vazquez, 2012), the ascending colon had three ansae (proximal, spiral and distal). Also in agreement with the literature of the domestic ruminants, the spiral ansa consisted of centripetal gyri, a central flexure and centrifugal gyri (Barone, 1997; Nomina Anatomica Veterinaria, 2012). The small/large intestine ratio (1.69) is less than the 1.9–2.7 ratio of the browsers (Hofmann, 1989). The ratio of 1.3–2.0 in the strictly browser species as giraffe and okapi (Perez et al., 2009) is even below this range. Brown brocket deer, other browser deer, have a ratio of 2.0 (Perez and Vazquez, 2012). In contrast, grazers as the domestic cattle achieve ratios of 4.0–5.5, even greater than the range of 4.0–5.0 given by Hofmann (1989) for typical grazers. However, long large intestines have also been observed in several grazing wild ruminant species (Hofmann, 1999; Clauss et al., 2005; Perez et al., 2008). Therefore, it seems that rather than characterizing a difference between feeding types, the observed differences in intestinal ratios more likely set cattle-like ruminants apart from other ruminant species. The anatomy of the gastrointestinal tract of axis deer agrees with reports on its natural feeding habits (Rodgers, 1988; Van Wieren, 1996) and with the classification of Hofmann (1985) as an intermediate feeder. Its morphology of intermediate-type deer allowed to consume a wide range of vegetable diets that emphasize the evolutionary flexibility of the ruminant digestive system. Acknowledgements Authors acknowledge to Divisi on de Fauna from the Ministerio de Ganaderıa, Agricultura y Pesca, and to Parque Anchorena of the Presidencia de la Rep ublica.
48
References Barone, R., 1997: Anatomie comparee des mammiferes domestiques. Tome 3, Edit. 3 (Splanchnologie I. Appareil digestif, appareil respiratoire). Paris: Vigot Freres. Clauss, M., J. Hummel, F. Vercammen, and W. J. Streich, 2005: Observations on the macroscopic digestive anatomy of the Himalayan Tahr (Hemitragus jemlahicus). Anat. Histol. Embryol. 34, 276–278. Clauss, M., R. R. Hofmann, J. Hummel, J. Adamczewski, K. Nygren, C. Pitra, and S. Reese, 2006: The macroscopic anatomy of the omasum of free-ranging moose (Alces alces) and muskoxen (Ovibos moschatus) and a comparison of the omasal laminal surface area in 34 ruminant species. J. Zool. 270, 346–358. Clauss, M., R. R. Hofmann, J. Fickel, W. J. Streich, J. Hummel, and G. W. Foundation, 2009: The intraruminal papillation gradient in wild ruminants of different feeding types: implications for rumen physiology. J. Morphol. 270, 929–942. Clauss, M., R. R. Hofmann, W. J. Streich, J. Fickel, and J. Hummel, 2010: Convergence in the macroscopic anatomy of the reticulum in wild ruminant species of different feeding types and a new resulting hypothesis on reticular function. J. Zool. 281, 12–25. Forsyth, D. M., and K. W. Fraser, 1999: Seasonal changes in the rumen morphology of Himalayan tahr (Hemitragus jemlahicus) in the two thumb range. South Island, New Zealand. J. Zool. 249, 241–248. Fraser, K. W., 1996: Comparative rumen morphology of sympatric sika deer (Cervus nippon) and red deer (C. elaphus scoticus) in the Ahimanawa and Kaweka Ranges, central North Island, New Zealand. Oecologia. 105, 160–166. Hemmoda, A. S. K., and R. Berg, 1980: Gross-anatomical Studies on the Ruminal Pillar System of the Egyptian Water Buffalo (Bos bubalis L.). Anat. Histol. Embryol. 2, 148–154. Hofmann, R. R., 1969: Zur Topographie und Morphologie des Wiederk€auermagens im Hinblick auf seine Funktion (nach vergleichenden Untersuchungen an Material ostafrikanischer Wildarten). J. Vet. Med. Suppl. 10, 1–180. Hofmann, R. R., 1973: The Ruminant Stomach. Nairobi: East African Literature Bureau. Hofmann, R. R., 1985: Digestive physiology of the deer – their morphophysiological specialisation and adaptation. R. Soc. N. Z. Bull. 22, 393–407. Hofmann, R. R., 1988: Morphophysiological evolutionary adaptations of the ruminant digestive system. In: Aspects of Digestive Physiology in Ruminants. (A. Dobson and M. Dobson, eds). Ithaca, NY: Cornell University Press. pp. 1–20. Hofmann, R. R., 1989: Evolutionary steps of ecophysiological adaptation and diversification of ruminants: a comparative view of their digestive system. Oecologia. 78, 443–457. Hofmann, R. R., 1999: Functional and comparative digestive system anatomy of Arctic ungulates. Rangifer. 20, 71–81.
© 2014 Blackwell Verlag GmbH Anat. Histol. Embryol. 44 (2015) 43–49
W. P erez, S. Erdogan and R. Ungerfeld
Hofmann, R. R., and B. Matern, 1988: Changes in gastrointestinal morphology related to nutrition in giraffes (Giraffa camelopardalis): a comparison of wild and zoo specimens. Int. Zoo. Yb. 27, 168–176. Hofmann, R. R., and K. Nygren, 1992: Ruminal mucosa as indicator of nutritional status in wild and captive moose. Alces Suppl. 1, 77–83. Hofmann, R. R., and D. R. M. Stewart, 1972: Grazers and browsers: a classification based on the stomach structure and feeding habits of East African ruminants. Mammalia. 36, 226–240. Josefsen, T. D., T. H. Aagnes, and S. D. Mathiesen, 1996: Influence of diet on the morphology of the ruminal papillae in reindeer calves (Rangifer tarandus). Rangifer. 16, 119–128. Kay, R. N. B., W. V. Engelhardt, and R. G. White, 1980: The digestive physiology of wild ruminants. In: Digestive Physiology and Metabolism in Ruminants. (Y. Ruckebusch and P. Thivend, eds). Lancaster: MTP Press. pp. 743–762. K€ onig, R., R. R. Hofmann, and G. Geiger, 1976: Differentiellmorphologische Untersuchungen der resorbierenden schleimhautoberfla che des pansens beim rehwild (Capreolus capreolus) im sommer und winter. Eur. J. Wildl. Res. 22, 191–196. Lentle, R. G., I. M. Henderson, and K. J. Stafford, 1996: A multivariate analysis of rumen papillary size in red deer (Cervus elaphus). Can. J. Zool. 74, 2089–2094. M€ unnich, J., G. G€abel, and H. Pfannkuche, 2008: Intrinsic ruminal innervation in ruminants of different feeding types. J. Anat. 213, 442–451. Nomina Anatomica Veterinaria, 2012: International Committee on Veterinary Gross Anatomical Nomenclature (I.C.V.G.A.N.), 5th edn revised. Hannover, Germany: Nomina Anatomica Veterinaria. Perez, W., and R. Ungerfeld, 2012: Gross anatomy of the stomach of the pampas deer, Ozotoceros bezoarticus (Artiodactyla: Cervidae). Zoologia (Curitiba). 29, 337–342. Perez, W., and N. Vazquez, 2012: Gross anatomy of the gastrointestinal tract in the Brown Brocket deer (Mazama gouazoubira). J. Morphol. Sci. 29, 148–150. Perez, W., M. Clauss, and R. Ungerfeld, 2008: Observations on the macroscopic anatomy of the intestinal tract and its
© 2014 Blackwell Verlag GmbH Anat. Histol. Embryol. 44 (2015) 43–49
Anatomy of Gastrointestinal Tract in Axis Deer
mesenteric folds in the pampas deer (Ozotoceros bezoarticus). Anat. Histol. Embryol. 37, 317–321. Perez, W., M. Lima, and M. Clauss, 2009: Gross anatomy of the intestine in the giraffe (Giraffa camelopardalis). Anat. Histol. Embryol. 38, 432–435. Pfannkuche, H., M. Schemann, and G. G€abel, 2002: Ruminal muscle of sheep is innervated by non-polarized pathways of cholinergic and nitrergic myenteric neurones. Cell Tissue Res. 309, 347–354. Rodgers, W. A., 1988: The wild grazing ungulates of India: an ecological review. In: Rangelands—Resource and Management. (P. Singh and P. S. Pathak, eds). Proceedings of the National Rangeland Symposium. Jhansi: IGFRI. pp. 404–419. Sakata, T., and H. Tamate, 1978: Rumen epithelial cell proliferation accelerated by rapid increase in intraruminal butyrate. J. Dairy Sci. 61, 1109–1113. Sakata, T., and H. Tamate, 1979: Rumen epithelial cell proliferation accelerated by propionate and acetate. J. Dairy Sci. 62, 49–52. Sander, E. G., R. G. Warner, H. N. Harrison, and J. K. Loosli, 1959: The stimulatory effect of sodium butyrate and sodium propionate on the development of the rumen mucosa in the young calf. J. Dairy Sci. 42, 1600–1605. Steinheim, G., L. A. Nordheim, R. B. Weladji, Ø. Holand, and T. Adnøy, 2003: Digestive tract anatomy of Norwegian sheep: difference between breeds. Acta Agric. Scand. A Anim. Sci. 3, 155–158. Teixeira, A. F., W. K€ uhnel, P. Vives, and T. Wedel, 2009: Functional morphology of unguiculiform papillae of the reticular groove in the ruminant stomach. Ann. Anat. 191, 469–476. Van Wieren, S. E., 1996: Browsers and grazers: foraging strategies in ruminants. In: Digestive Strategies in Ruminants and Nonruminants: Thesis Landbouw. (S. E. Van Wieren, ed.). Wageningen, The Netherlands: University of Wageningen. Warner, R. G., W. P. Flatt, and J. K. Loosli, 1956: Dietary factors influencing the development of the ruminant stomach. J. Agric. Food. Chem. 4, 788–792.
49
