1 Institution: Aarhus University, Department of Animal Science 1 2 Title: Quantitative Macroscopic Anatomy of the Giraffe (Giraf
Total Page：16
File Type：pdf, Size：1020Kb
Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch Year: 2016 Quantitative macroscopic anatomy of the giraffe (giraffa camelopardalis) digestive tract Sauer, C ; Bertelsen, M F ; Lund, P ; Weisbjerg, M R ; Clauss, Marcus Abstract: Quantitative data on digestive anatomy of the world’s largest ruminant, the giraffe, are scarce. Data were collected from a total of 25 wild-caught and 13 zoo-housed giraffes. Anatomical measures were quantified by dimension, area or weight and analysed by allometric regression. The majorityof measures scaled positively and isometrically to body mass. Giraffes had lower tissue weight of all stomach compartments and longer large intestinal length than cattle. When compared to other ruminants, the giraffe digestive tract showed many of the convergent morphological adaptations attributed to browsing ruminants, for example lower reticular crests, thinner ruminal pillars and smaller surface area of the omasal laminae. Salivary gland weight of the giraffe, however, resembled that of grazing ruminants. This matches a previous finding of similarly small salivary glands in the other extant giraffid, theokapi (Okapia johnstoni), suggesting that not all convergent characteristics need be expressed in all species and that morphological variation between species is a combination of phylogenetic and adaptational signals. DOI: https://doi.org/10.1111/ahe.12201 Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-125912 Journal Article Accepted Version Originally published at: Sauer, C; Bertelsen, M F; Lund, P; Weisbjerg, M R; Clauss, Marcus (2016). Quantitative macroscopic anatomy of the giraffe (giraffa camelopardalis) digestive tract. Anatomia, Histologia, Embryologia, 45(5):338-349. DOI: https://doi.org/10.1111/ahe.12201 1 Institution: Aarhus University, Department of Animal Science 2 3 Title: Quantitative macroscopic anatomy of the giraffe (Giraffa camelopardalis) digestive tract 4 5 Cathrine Sauer1,2 6 Mads F. Bertelsen2 7 Peter Lund1 8 Martin R. Weisbjerg1 9 Marcus Clauss3 10 11 1Department of Animal Science, Aarhus University, AU Foulum, Blichers Allé 20, PO Box 50, DK- 12 8830 Tjele, Denmark. 13 2Center for Zoo and Wild Animal Health, Copenhagen Zoo, Roskildevej 38, DK-2000 Frederiksberg, 14 Denmark. 15 3Clinic for Zoo Animals, Exotic Pets and Wildlife, Vetsuisse Faculty, University of Zurich, 16 Winterthurerstr. 260, CH-8057 Zurich, Switzerland. 17 18 Corresponding author email: [email protected] 19 20 Number of figures in manuscript: 7 21 Number of tables in manuscript: 7 22 1 23 Summary 24 Quantitative data on digestive anatomy of the world’s largest ruminant, the giraffe, are scarce. Data 25 were collected from a total of 25 wild caught and 13 zoo housed giraffes. Anatomical measures were 26 quantified by dimension, area or weight, and analyzed by allometric regression. The majority of 27 measures scaled positively and isometrically to body mass. Giraffes had lower tissue weight of all 28 stomach compartments and longer large intestinal length than cattle. When compared to other 29 ruminants, the giraffe digestive tract showed many of the convergent morphological adaptations 30 attributed to browsing ruminants, e.g., lower reticular crests, thinner ruminal pillars and smaller 31 surface area of the omasal laminae. Salivary gland weight of the giraffe, however, resembled that of 32 grazing ruminants. This matches a previous finding of similarly small salivary glands in the other 33 extant giraffid, the okapi (Okapia johnstoni) suggesting that not all convergent characteristics need 34 be expressed in all species and that morphological variation between species is a combination of 35 phylogenetic and adaptational signals. 36 37 Introduction 38 Our current knowledge of the digestive anatomy and physiology of ruminants is generally based on a 39 few but thoroughly studied livestock species, while only selective descriptions and scant quantitative 40 data are available for non-domestic species. Domestic ruminants are grazers or intermediate feeders 41 according to the classification introduced by Hofmann and Stewart (1972) and have ‘cattle-type’ 42 digestive tracts according to a more recently proposed classification of ruminants as either ‘cattle- 43 type’ or ‘moose-type’ based on digestive tract anatomy and physiology (Clauss et al., 2010a; 44 Dittmann et al., 2015). Briefly, ‘cattle-type’ ruminants have stratified rumen contents, a fast 45 reticuloruminal fluid throughput, a relatively large omasum, deep reticular crests and thick rumen 46 pillars. In contrast, ‘moose-type’ ruminants have homogenous rumen contents, a slower fluid 47 throughput, a relatively small omasum, low reticular crests and thin rumen pillars (Clauss et al. 48 2010a). Whereas ‘moose-types’ are usually strict browsers, ‘cattle-types’ may include varying 49 amounts of grass in their diet to the effect that they are either considered strict grazers or mixed 50 feeders (Codron and Clauss, 2010). The difference between these two types is currently thought to be 51 related to a difference in the amount and viscosity of saliva they produce: whereas the ‘moose-type’ 52 is thought to produce lesser amounts of a more proteinaceous (and hence viscous) saliva due to the 53 inclusion of tannin-binding proteins, the ‘cattle-type’ produces larger amounts of a more watery 2 54 saliva (Hofmann et al. 2008). The success of the ‘cattle-type’ is thought to lie in the more intensive 55 harvest of microbes growing in the rumen by the increased 'wash-out' effect of the high fluid 56 throughput (Dittmann et al. 2015). Of the browsing or ‘moose-type’ ruminants, only the moose 57 (Alces alces) and roe deer (Capreolus capreolus) have been studied in detail (e.g., Hofmann et al., 58 1976; Hofmann and Nygren, 1992a, 1992b), while comprehensive information on the world’s largest 59 ruminant, the giraffe, is scarce. A few reports provide quantitative data on the digestive anatomy of 60 the giraffe (e.g., Hofmann, 1973; Maloiy et al., 1982; Pérez et al., 2009), but these studies are 61 generally based on very few individuals or lack information about body mass (BM). A more 62 comprehensive quantitative description of the digestive system of the giraffe would allow a better 63 comparison of giraffes to other ruminants such as cattle, and facilitate a more detailed understanding 64 of the overall comprehension of the evolutionary diversification of ruminants. 65 The first aim of this study was to provide solid data on the gross anatomy of the gastrointestinal tract 66 of the giraffe using selected measures previously used to describe the ruminant digestive system 67 (e.g., Hofmann, 1973; Clauss et al., 2005, 2006a) and to determine the scaling relationship between 68 BM and these anatomical measures. It was hypothesized that measures would scale isometrically to 69 BM, i.e., linear dimensions to BM0.33, area measurements to BM0.67, and weight measurements to 70 BM1.00 based on simple geometric considerations (Peters, 1983). Further, it was hypothesized that the 71 digestive system of the giraffe would show morphological adaptations similar to those described for 72 ruminants with a ‘moose-type’ digestive tract, and be notably different from ruminants with a ‘cattle- 73 type’ digestive tract . Therefore, the second aim of this study was to test this hypothesis through 74 comparison with other ruminant species. 75 Materials and methods 76 Data were collected from 25 wild and 13 captive giraffes, though not every measure was obtained 77 from every individual due to practical limitations or time constraints. Due to logistical 78 considerations, the wild giraffes were caught in South Africa or Namibia and housed by Wildlife 79 Assignments International Ltd, Hammanskraal, South Africa, for approximately 2 months before the 80 dissection. During this period, the giraffes were group housed and received a diet of fresh locally cut 81 savanna browse, leafy lucerne hay, and BoskosTM pellets (WES Enterprises (Pty) Ltd., South Africa). 82 Water was freely available. The wild giraffes were all euthanized following physiological 83 experiments conducted by the Danish Cardiovascular Giraffe Research project. Permission for 84 euthanasia was granted by the Gauteng Province of South Africa. 3 85 Zoo giraffes from six Danish and one Swedish zoo were either culled for management reasons or 86 because of chronic lameness due to osteoarthritis. These animals were fed diets consisting of hay 87 (mainly alfalfa, but in a few cases grass-based), various concentrate pellets and as much browse as 88 possible. Limited amounts of other feeds including BoskosTM pellets, beet pellets, linseeds, oats, 89 maize and various fruits and vegetables were used by individual institutions. Two newly born zoo 90 giraffe calves were opportunistically included in the study. One was euthanized because of severe 91 trauma, the other died perinatally. 92 Giraffe taxonomy is in flux, but using current nomenclature (Brown et al., 2007), 3 subspecies of 93 giraffes, as well as 5 hybrids were represented in the study. Demographic information about 94 individual giraffes is listed in Table 1. 95 The dissection protocol was initiated within 30 minutes of euthanasia of the animals, except for the 96 two giraffe calves, which were stored overnight at 5°C degrees prior to dissection. BM was obtained 97 by weighing the giraffe in an upright position, using straps and a hanging electronic