High fibre selection by roe deer (Capreolus capreolus): evidence of ruminal microbiome adaption to seasonal and geographical differences in nutrient composition
Sarah-Alica Dahl
A C , Martina Hudler A , Wilhelm Windisch B , Carmen Bolduan B , Daniel Brugger B and Andreas König A
+ Author Affiliations
- Author Affiliations
A Wildlife Biology and Management Unit, Technical University of Munich, Hans-Carl-von-Carlowitz-Platz 2, 85354 Freising, Germany.
B Chair of Animal Nutrition, Technical University of Munich, Liesel-Beckmann-Straße 2, 85354 Freising, Germany.
C Corresponding author. Email: dahl@wzw.tum.de
Animal Production Science 60(10) 1303-1314 https://doi.org/10.1071/AN19376
Submitted: 7 July 2019 Accepted: 14 January 2020 Published: 11 May 2020
Abstract
Context. The European roe deer owes its ability to digest fibre to its microbiome. This is made up of many different species at different levels of abundance and with different differentiations. In Europe, the roe deer is often classified as a so-called ‘concentrate selector’. This term has often been interpreted by different researchers to mean a selector of either protein- or energy-rich food. According to various studies, this selection behaviour is due to the low abundance of fibre-degrading microorganisms.
Aims. The aim of the present study was to determine the concentration of crude nutrients in the rumen of roe deer, with the focus on the fibre fractions, and to show changes among seasons and between habitats. Furthermore, the aim was to find out how far the composition of the ruminal microbiota adapts to these changes.
Methods. From 2011 to 2014, we collected the rumens of 245 roe deer in two Bavarian habitat types, a forest and an agricultural habitat. The crude nutrient contents and the size of the total microbiome and the proportions of individual genera were determined in the rumen content.
Key results. The average annual concentration of crude fibre in the ingested food is 26–30% and this rises to 38% in certain months. The forest roe deer had the highest proportions of crude fibre in their food and the concentrations of other nutrients were also highly dependent on the season and habitat. Furthermore, the animals also have far less protein in their rumen content than often assumed. The total number of microorganisms in the rumens of the forest deer is significantly higher than in animals living in the agricultural area. The number of microorganisms was highest in the forest roe deer in winter, and in the roe deer from the agricultural area in summer. Clear connections can also be seen between individual groups of microorganisms and particular crude nutrients. The high crude-fibre concentration leads to a high number of fibre-degrading microorganisms, such as, for example, anaerobic fungi or the Ruminococcus flavefaciens.
Conclusions. The results showed a high adaptability of the animals to a fibre-rich diet. The microbiome adapts very well to the respective nutrient availabilities. This, in turn, is what allows the roe deer to adapt so readily to diverse habitats and environmental conditions.
Implications. Due to the generally high concentrations of fibre, combined with the high numbers of fibre-degraders in the rumen, we suggest that, from now on, we should talk of a roe deer as being a ‘selector’ or ‘browser’ rather than a ‘concentrate selector’.
Additional keywords: bacteria, carbohydrates, fungi, nutrient requirement, ruminant.
References
Abbas F, Picot D, Merlet J, Cargnelutti B, Lourtet B, Angibault J-M, Daufresne T, Aulagnier S, Verheyden H (2013) A typical browser, the roe deer, may consume substantial quantities of grasses in open landscapes. European Journal of Wildlife Research 59, 69–75.| A typical browser, the roe deer, may consume substantial quantities of grasses in open landscapes.Crossref | GoogleScholarGoogle Scholar |
Alber U (1990) Botanische Panseninhaltsanalyse bei Rehwild (Capreolus capreolus) im Staatlichen Bayerischen Forstamt Bodenmais. Diploma Thesis. Georg-August-Universität, Göttingen, Germany.
Anke M, Dittrich G, Groppel B, Schäfer U, Müller R, Hoppe C (2007) Zusammensetzung und Aufnahme von Winteräsung durch Reh-, Muffel-, Dam- und Rotwild. In ‘Beiträge zur Jagd- und Wildforschung. Vol. 32’. (Ed. M Stubbe) pp. 379–398.
Barančeková M, Krojerová-Prokešová J, Šustr P, Heurich M (2010) Annual changes in roe deer (Capreolus capreolus L.) diet in the Bohemian Forest, Czech Republic/Germany. European Journal of Wildlife Research 56, 327–333.
| Annual changes in roe deer (Capreolus capreolus L.) diet in the Bohemian Forest, Czech Republic/Germany.Crossref | GoogleScholarGoogle Scholar |
Barboza PS, Parker K, Hume ID (2009) ‘Integrative Wildlife Nutrition.’ (Springer-Verlag: Berlin, Germany)
Behrend A (1999) Kinetik des Ingestaflusses bei Rehen und Mufflons im saisonalen Verlauf. Humbold-Universität Berlin, Germany.
Belovsky GE (1978) Diet optimization in a generalist herbivore: the moose. Theoretical Population Biology 14, 105–134.
| Diet optimization in a generalist herbivore: the moose.Crossref | GoogleScholarGoogle Scholar | 741393PubMed |
Briedermann L, Dittrich G, Lockow K-W (1988) Rotwild Cervus elaphus L. In ‘Buch der Hege Band 1 Haarwild’. (Ed. H Stubbe) pp. 2–57. (Verlag Harri Deutsch: Thun, Frankfurt am Main, Germany)
Brüggemann J, Giesecke D, Walser-Kärst K (1967) Beiträge zur Wildbiologie und vergleichenden Tierphysiologie. II. Mikroorganismen im Pansen von Rothirsch und Reh. Zeitschrift fur Tierphysiologie, Tierernahrung und Futtermittelkunde 23, 143–151.
| Beiträge zur Wildbiologie und vergleichenden Tierphysiologie. II. Mikroorganismen im Pansen von Rothirsch und Reh.Crossref | GoogleScholarGoogle Scholar | 5634228PubMed |
Buchgraber, A (2005) Nahrungsangebot für Rehwild auf Grünland- und Ackerflächen, Östereichische Jägertagung 15 und 16 Feburar 2005. (Raumberg-Gumpenstein: Irdning, Styria, Austria)
Chen H, Ma J, Li F, Sun Z, Wang H, Luo L, Li F (1998) Seasonal composition and quality of red deer Cervus elaphus diets in northeastern China. Acta Theriologica 43, 77–94.
| Seasonal composition and quality of red deer Cervus elaphus diets in northeastern China.Crossref | GoogleScholarGoogle Scholar |
Clauss M (2010) ‘Artgerechte Fütterung der Wildtiere: was ist fachlich Vertretbar. 16. Österreichische Jägertagung.’ (Raumberg-Gumpenstein)
Dahl S-A (2015) Erfassung von Fraßpräferenzen und Habitatnutzung von Elchen (Alces alces) im polaren Raum. Masters Thesis, University of Hamburg, Germany.
Deutz A (2009) Untersuchungen zum Auftreten von Nierenveränderungen bei gefüttertem und ungefütterten Rehwild. Gesellschaft für Wildtier und Lebensraum, St Lambrecht, Mödling, Austria.
Dissen J, Hartfiel W (1985) Beobachtungen zum Äsungsverhalten sowie Untersuchungen zur Nährstoffverdaulichkeit von Rehwild. Zeitschrift fur Jagdwissenschaft 31, 83–91.
Djordjevic N, Popovic Z, Grubic G (2006) Chemical composition of the rumen contents in roe deer (Capreolus capreolus) as potetial quality indicator of their feeding. Journal of Agricultural Sciences 51, 133–140.
| Chemical composition of the rumen contents in roe deer (Capreolus capreolus) as potetial quality indicator of their feeding.Crossref | GoogleScholarGoogle Scholar |
Drescher-Kaden U, Seifelnasr EA (1977) Untersuchungen zum Verdauungstrakt von Rehwild, Damwild und Mufflon. Mitteilung 2: Rohnährstoffe im Panseninhalt von Reh, Damhirsch und Mufflon. Zeitschrift fur Jagdwissenschaft 23, 6–11.
Drożdż A (1973) Intake and digestibility of natural feeds by roe-deer. Acta Theriologica 18, 81–91.
| Intake and digestibility of natural feeds by roe-deer.Crossref | GoogleScholarGoogle Scholar |
Duncan P, Tixier H, Hofmann RR, Lechner-Doll M (1998) Feeding strategies and the physiology of digestion in roe deer. In ‘The European roe deer: the biology of success’. pp. 91–116. (Scandinavian University Press: Oslo, Norway)
Enzinger W, Hartfiel W (1998) Auswirkungen gesteigerter Energie- und Proteingehalte des Futters auf Fermentationsprodukte, Fauna und Schleimhaut des Pansens von Wildwiederkäuern in Vergleich zu Hauswiederkäuern. Zeitschrift fur Jagdwissenschaft 44, 201–220.
Esser W (1958) Beitrag zur Untersuchung der Äsung des Rehwildes. Zeitschrift fur Jagdwissenschaft 4, 1–40.
Felton AM, Felton A, Raubenheimer D, Simpson SJ, Krizsan SJ, Hedwall P, Stolter C (2016) The nutritional balancing act of a large herbivore: an experiment with captive moose (Alces alces L.). PLoS One 11, e0150870
| The nutritional balancing act of a large herbivore: an experiment with captive moose (Alces alces L.).Crossref | GoogleScholarGoogle Scholar | 26986618PubMed |
Felton AM, Wam HK, Stolter C, Mathisen KM, Wallgren M (2018) The complexity of interacting nutritional drivers behind food selection, a review of northern cervids. Ecosphere 9, e02230
| The complexity of interacting nutritional drivers behind food selection, a review of northern cervids.Crossref | GoogleScholarGoogle Scholar |
Hanauer MJ (2017) Experimental study on the effect of dose and source of copper supplementation on copper metabolism, rumen microbiota, and rumen fermentation characteristics in cannulated cows. Doctoral Thesis, Technical University of Munich, Germany.
Henderson G, Cox F, Ganesh S, Jonker A, Young W, Collaborators GRC, Janssen PH (2015) Rumen microbial community composition varies with diet and host, but a core microbiome is found across a wide geographical range. Scientific Reports 5, 14567–13.
| Rumen microbial community composition varies with diet and host, but a core microbiome is found across a wide geographical range.Crossref | GoogleScholarGoogle Scholar | 26449758PubMed |
Hewison AJM, Morellet N, Verheyden H, Daufresne T, Angibault J-M, Cargnelutti B, Merlet J, Picot D, Rames J-L, Joachim J, Lourtet B, Serrano E, Bideau E, Cebe N (2009) Landscape fragmentation influences winter body mass of roe deer. Ecography 32, 1062–1070.
| Landscape fragmentation influences winter body mass of roe deer.Crossref | GoogleScholarGoogle Scholar |
Hofmann RR (1978) Die Stellung der europäischen Wildwiederkäuer im System der Äsungstypen. In ‘Wildbiologische Informationen für den Jäger. Vol. 1’. (Ed. E Penkner) pp. 9–18. (Ferdinand Enke Verlag: Stuttgart, Germany)
Hofmann RR (1989) Evolutionary steps of ecophysiological adaption and diversification of ruminants: a comperative view if their digestives system. Oecologia 78, 443–457.
| Evolutionary steps of ecophysiological adaption and diversification of ruminants: a comperative view if their digestives system.Crossref | GoogleScholarGoogle Scholar | 28312172PubMed |
Jiang Z, Hudson J (1996) Digestive response of wapiti Cervus elaphus canadensis to seasonal forage. Acta Theriologica 41, 415–423.
| Digestive response of wapiti Cervus elaphus canadensis to seasonal forage.Crossref | GoogleScholarGoogle Scholar |
Jones GM (1972) Chemical factors and their relation to feed intake regulation in ruminants. A review. Canadian Journal of Animal Science 52,
| Chemical factors and their relation to feed intake regulation in ruminants. A review.Crossref | GoogleScholarGoogle Scholar |
Klötzli F (1965) Qualität und Quantität der Rehäsung. PhD Thesis. Eidgenössische Technische Hochschule Zürich: Zürich, Switzerland.
König A, Scheingraber M, Mitschke J (2016) ‘Energiegehalt und Qualität der Nahrung von Rehen (Capreolus capreolus) im Jahresverlauf in zwei unterschiedlich geprägten Habitaten.’ (Zentrum Wald-Forst-Holz: Freising, Germany)
König A, Hudler M, Dahl S-A, Bolduan C, Brugger D, Windisch W (2020) Response of roe deer (Capreolus capreolus) to seasonal and local changes in dietary energy content and quality. Animal Production Science
| Response of roe deer (Capreolus capreolus) to seasonal and local changes in dietary energy content and quality.Crossref | GoogleScholarGoogle Scholar |
Kurt F (1991) ‘Das Reh in der Kulturlandschaft.’ (Verlag Paul Parey: Hamburg, Germany)
Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annual Review of Ecology and Systematics 11, 119–161.
| Herbivory in relation to plant nitrogen content.Crossref | GoogleScholarGoogle Scholar |
Millen DD, De Beni Arrigoni M, Lauritano Pacheco RD (2016) ‘Rumenology.’ (Springer-Verlag: Switzerland)
Onderscheka K (1999) ‘Das Rehwild: seine Ernährung und Fütterung.’ (Landesjagdverband Bayern e.V.: Nürnberg, Germany)
Popovic Z, Djordjevic N, Djordjevic M, Grubic G, Stojanovic B (2009) Estimation of the quality of the nutrition of roe deer based on chemical composition of the rumen content. Acta Veterinaria 59, 653–663.
| Estimation of the quality of the nutrition of roe deer based on chemical composition of the rumen content.Crossref | GoogleScholarGoogle Scholar |
Raubenheimer D, Simpson SJ, Le Couteur DG, Solon-Biet SM, Coogan SCP (2016) Nutritional ecology and the evolution of aging. Experimental Gerontology 86, 50–61.
| Nutritional ecology and the evolution of aging.Crossref | GoogleScholarGoogle Scholar | 27094469PubMed |
Reimoser F (2005) ‘Rehwild in der Kulturlandschaft. 11. Österreichische Jägertagung.’ Raumberg-Gumpenstein. Höhere Bundeslehr- und Forschungsanstalt für Landwirtschaft, Irdning, Styria, Austria.
Reimoser F (2006) Begleitforschung zum Projekt Nationalparkjagden im Gasteinertal. Forschungsinstitut für Wildtierkunde und Ökologie, Wien, Austria.
Ricci S, Sandfort R, Pinior B, Mann E, Wetzels SU, Stalder G (2019) Impact of supplemental winter feeding on ruminal microbiota of roe deer Capreolus capreolus. Wildlife Biology 2019, 1–11.
| Impact of supplemental winter feeding on ruminal microbiota of roe deer Capreolus capreolus.Crossref | GoogleScholarGoogle Scholar |
Schmidl C (1996) Botanische und chemische Panseninhaltsanalysen, chemische Blutuntersuchungen und Untersuchungen der Schwermetallbelastung beim Rehwild. Veterinärmedizinische Universität Wien, Austria.
Senchik A, Tikhonchuk P, Ran O, Bochkarev S (2019) A description of principal forage crops used for extra nutririon of wild ungulates (Sus scrofa ussuricus, Alces alces cameloides, Cervus elaphus xanthopygus, Capreolus pyrargus pallas) in Siberia and the far east of Russia. In ‘The 12th international syposium on wild boar and other suids’, Czech Republic.
Sommer A (2004) Stoffwechsel der Wildwiederkäuer. In ‘Tagung für die Jägerschaft. Irdning’. pp. 3–6. (Bundesanstalt für Apenländische Landwirtschaft Gumpenstein)
Stolter C, Ball JP, Julkunen-Tiitto R, Lieberei R, Ganzhorn JU (2005) Winter browsing of moose on two different willow species: food selection in relation to plant chemistry and plant response. Canadian Journal of Zoology 83, 807–819.
| Winter browsing of moose on two different willow species: food selection in relation to plant chemistry and plant response.Crossref | GoogleScholarGoogle Scholar |
Terry SA, Badhan A, Wang Y, Chaves AV, McAllister TA (2019) Fibre digestion by rumen microbiota - a review of recent metagenomic and metatranscriptomic studies. Canadian Journal of Animal Science 99, 678–692.
| Fibre digestion by rumen microbiota - a review of recent metagenomic and metatranscriptomic studies.Crossref | GoogleScholarGoogle Scholar |
Tixier H, Duncan P (1996) Are European roe deer browsers? Revue d’Ecologie. La Terre et la Vie 51, 3–17.
Van Soest PJ (1982) ‘Nutritional ecology of the ruminant.’ (O & B Books, Inc.: Corvallis, OR)
Van Soest PJ (1996) Allometry and ecology of feeding behaviour and digestive capacity in herbivores: a review. Zoo Biology 15, 455–479.
| Allometry and ecology of feeding behaviour and digestive capacity in herbivores: a review.Crossref | GoogleScholarGoogle Scholar |
VDLUFA (2012) ‘VDLUFA-methods book 3: the chemical analysis of feedstuffs.’ (VDLUFA-Verlag: Darmstadt, Germany)
Veith S (1992) Nahrungswahl von Rehen in einem Revier der Zentralalpen. Diploma Thesis. Ludwig-Maximilians-Universität, München, Germany.
