The survival of a Malagasy lemur species Propithecus verreauxi coquereli in captivity [Elektronische Ressource] : the vital role of a self-selected plant diet / von Annette Abhau
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The survival of a Malagasy lemur species Propithecus verreauxi coquereli in captivity [Elektronische Ressource] : the vital role of a self-selected plant diet / von Annette Abhau

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325 Pages
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The survival of a Malagasy lemur speciesPropithecus verreauxi coquereliin captivity:The vital role of a self-selected plant dietVon der Fakultät für Lebenswissenschaftender Technischen Universität Carolo-Wilhelminazu Braunschweigzur Erlangung des Grades einerDoktorin der Naturwissenschaften(Dr. rer. nat.)genehmigteD i s s e r t a t i o nvon Annette Abhauaus Mülheim an der Ruhr1. Referent: Professor Dr. Thomas Hartmann2. Referent: Professor Dr. Dieter Strack3. Referentin: Professor Dr. Joyce A. Powzykeingereicht am: 19.12.2006mündliche Prüfung (Disputation) am: 25.04.2007Druckjahr 2007Vorveröffentlichungen der DissertationTeilergebnisse aus dieser Arbeit wurden mit Genehmigung der Fakultät fürLebenswissenschaften, vertreten durch den Mentor der Arbeit, in folgenden Beiträgen vorabveröffentlicht:Vorträge:Abhau, A.: Secondary compounds in the feeding plants of Propithecus verreauxi coquereli.Duke University Lemur Center, N.C., USA (1997).Abhau, A.: Secondary compounds in the feeding plants of Propithecus verreauxi coquereli.2. Kurt-Mothes-Doktoranden-Workshop, „Sekundärstoffwechsel“,IPB, Halle / Saale, Deutschland (1998).For Marcella and Tiberius«C’est principalement le sens de l’odorat, dont l’étude vient de nous occuper, qui guideles Indrisinés dans le choix de leurs aliments; le goût y est peu de chose, car, le plussouvent, c’est après avoir flairé un fruit ou une feuille qu’ils le rejettent sans l’avoirporté à leur bouche.

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The survival of a Malagasy lemur species
Propithecus verreauxi coquereli
in captivity:
The vital role of a self-selected plant diet
Von der Fakultät für Lebenswissenschaften
der Technischen Universität Carolo-Wilhelmina
zu Braunschweig
zur Erlangung des Grades einer
Doktorin der Naturwissenschaften
(Dr. rer. nat.)
genehmigte
D i s s e r t a t i o n
von Annette Abhau
aus Mülheim an der Ruhr1. Referent: Professor Dr. Thomas Hartmann
2. Referent: Professor Dr. Dieter Strack
3. Referentin: Professor Dr. Joyce A. Powzyk
eingereicht am: 19.12.2006
mündliche Prüfung (Disputation) am: 25.04.2007
Druckjahr 2007Vorveröffentlichungen der Dissertation
Teilergebnisse aus dieser Arbeit wurden mit Genehmigung der Fakultät für
Lebenswissenschaften, vertreten durch den Mentor der Arbeit, in folgenden Beiträgen vorab
veröffentlicht:
Vorträge:
Abhau, A.: Secondary compounds in the feeding plants of Propithecus verreauxi coquereli.
Duke University Lemur Center, N.C., USA (1997).
Abhau, A.: Secondary compounds in the feeding plants of Propithecus verreauxi coquereli.
2. Kurt-Mothes-Doktoranden-Workshop, „Sekundärstoffwechsel“,
IPB, Halle / Saale, Deutschland (1998).For Marcella and Tiberius
«C’est principalement le sens de l’odorat, dont l’étude vient de nous occuper, qui guide
les Indrisinés dans le choix de leurs aliments; le goût y est peu de chose, car, le plus
souvent, c’est après avoir flairé un fruit ou une feuille qu’ils le rejettent sans l’avoir
porté à leur bouche. En captivité, il est fort difficile de nourrir ces animaux; ils refusent
presque tous les aliments qu’on leur voit d’abord approcher de leur narines, puis
abandonner aussitôt sans y avoir goûté.»
(Milne Edwards A. et A. Grandidier,
1875. Vol. VI. Histoire Naturelle Des Mammifères, p.226)Acknowledgements i
Acknowledgements
I wish to thank my supervisor Prof. Dr. Thomas Hartmann (Institut für Pharmazeutische
Biologie der Technischen Universität Braunschweig), who has always supported my project
and spent many hours discussing my work. I am very happy that he said “yes” to the idea of
my project, yet the outcome was not clear at the time of starting.
I am greatly indebted to my co-corrector Prof. Dr. Dieter Strack (Leibniz-Institut für
Pflanzenbiochemie, IPB, Halle / Saale), who was very generous in supporting my analytical
work. All HPLC analyses were performed at his laboratory and he provided me with all the
necessary equipment. I would also like to thank his team, especially Dr. Alfred Baumert who
was invaluable in helping to solve any analytical problem, and Dr. Thomas Fester, who was
so kind in assisting with both the executing of the gel-electrophoresis experiments and getting
things organised in Halle.
My project could not have started without the invitation of Prof. Dr. Ken Glander to visit the
Duke University Lemur Center, previously known as Duke University Primate Center, North
Carolina, USA. His personal support and far-sightedness as director and as researcher were
decisive for the initiation and continuance of my project. I wish to express my extreme
gratitude to him and his wife Molly, who I knew to be a kind and generous person. I will
always keep Molly in my memory.
This work could not have been completed without the experience and help of numerous
researchers that were integral at various stages of the project:
Prof. Dr. Robert L. Wilbur at the Botany Greenhouses of the Duke University identified the
plant species I had collected from the outdoor enclosures at the Primate Center. Much respect
for both his kindness and his straightforwardness in assisting me to identify the plant species
collected. Dr. Beverly Calhoun at the Botany Greenhouses and Mike McGowan, Duke
University Phytotron, collected additional plant material for my analyses when I had already
returned to Germany.
I am largely obliged to all the scientists who took their time and resources for mass
spectrometric and NMR spectroscopic measurements for structure elucidation of the
numerous compounds I had isolated through HPLC analyses. I am indebted to their kindness
and their willingness to discuss spectra and any other problems:
So, I wish to thank Dr. Jürgen Schmidt (MS-Labor, IPB, Halle / Saale), who performed the
majority of mass spectrometric measurements as well as the LC-MS measurements. Various
additional mass spectrometric measurements were performed by Dr. Hans-Martin Schiebel
and Mrs. Doris Döring (MS-Labor der Chemischen Institute der Technischen Universität
Braunschweig), and by Dr. Thomas Dülcks (MS-Labor, Institut für Organische Chemie,
Universität Bremen).
Dr. Schiebel deserves a special note of appreciation for spending innumerable hours in
solving sophisticated problems within mass spectrometry, and helping me to get additional
contacts to solve new raising problems. And least I forget the wonderful tea-time at the mass
laboratory which was always a welcome opportunity to take part in fruitful discussions. Dr.
Schiebel also lent a hand for me to contact the team of Prof. Dr. D. Leibfritz (Institut für
Organische Chemie, Universität Bremen), which was closer to my residence and afforded me
more time with my family and children’s education. He also assisted me in contactingii Acknowledgements
Dr. Manfred Nimtz (Gesellschaft für biotechnologische Forschung, GBF, Braunschweig) and
regularly travelled between the Universities of Braunschweig and Bremen, all the while
plying me with much needed support and news from Braunschweig. This allowed me to meet
Dr. Thomas Dülcks, who performed additional mass spectrometric experiments and was
partner to engaging discussions.
GC and GC-MS measurements were performed by Dr. Ludger Witte (MS-Labor der
Chemischen Institute der Technischen Universität Braunschweig). I am indebted to his
support and astute discussions and I was deeply saddened to learn of his untimely death.
For NMR-spectroscopic measurements I am greatly obliged to Prof. Dr. Ludger Ernst (NMR-
Labor der Chemischen Institute der Technischen Universität Braunschweig), and his assistant
Mrs. Petra Holba-Schulz, for performing the majority of the NMR measurements. Prof. Ernst
spent much time to solve problems raising during the interpretation of the NMR spectra. At
the University of Bremen I received additional support from the team of Prof. Leibfritz: and
my thanks go out to Dr. Werner Offermann, Dipl. Ing. Johannes Stelten and Dr. Wienand
Willker.
For microbiological experiments I wish to thank the PanLabs Inc., and much gratitude to Dr.
Ulf Preuschoff and Dr. Samuel David, Solvay Arzneimittel GmbH, for their engagement in
making these experiments possible. My thanks go also to Dr. Thomas Vieregge (Zentrale
Einrichtung für Tierhaltung der Technischen Universität, Braunschweig), for his support in
performing microbiological assays, and it was he who introduced me to Dr. Marie-Luise Enss
(Medizinische Hochschule, Hanover, MHH), a most generous woman.
Thanks to Dr. Enss, that the plant mucilage detected in one of the major lemur food plants
could be isolated. We had numerous enlightened discussions on possible pharmacological
aspects related to the gastrointestinal tract. The initial GC analyses on the plant mucilage were
carried out at the laboratory of Dr. Blaskowitz and Dr. Kownatzki (MHH).
Additionally, I am much obliged to Dr. Manfred Nimtz (GBF, Braunschweig), who
performed the mass spectrometric experiments on the plant mucilage and took many hours
from his busy schedule to introduce me into carbohydrate chemistry.
I am greatly obliged to Prof. Dr. Manfred Coenen (Institut für Tierernährung der
Tierärztlichen Hochschule, Hanover), and Peter Rust, head of the laboratory, for investigating
the nutritional components of the food plants. Prof. Coenen provided me with grass meal, that
was utilised as auxiliary agent to press tablets with the groups of chemical compounds
identified in the lemur food.
I also wish to thank the team of Prof. Dr. Christel Müller-Goymann (Institut für
Pharmazeutische Technologie der Technischen Universität Braunschweig), for providing me
with the support and the equipment needed to further this investigation. And many thanks to
Mrs. Jahn, who helped me to press tablets for the proposed feeding choice experiments.
For the generous supply of Plantaginis ovatae testa and tannin albuminate and much desirable
literature, I wish to thank Dr. Falk Pharma GmbH, and Knoll Deutschland GmbH / BASF
Pharma, now Dr. Rentschler Arzneimittel GmbH & Co., respectively. I also wish to
acknowledge the pharmaceutical companies Athenstaedt GmbH & Co. KG, Dr. Gustav Klein,
and Dr. Loges & Co. GmbH, for providing me with the information needed for dosage
comparisons between their medicaments and the amounts of secondary compounds ingested
by the lemurs. For the provision of isolated chemical plant compounds for analytical purposes
(reference compounds) I am much obliged to Prof. Dr. G. G. Gross (Abteilung für Allgemeine
Botanik der Universität Ulm), and the team of Prof. Dr. Junei Kinjo (Kumamoto University,
Faculty of Pharmaceutical Sciences, Japan).
For all the proofreading and requests for literature, I am much obliged to Prof. Dr. Joyce
Powzyk, Wesleyan University, C.T., USA, and her husband Dr. Stephen Devoto. I met JoyceAcknowledgements iii
in Madagascar and enjoyed the visit to her research camp to observe free-ranging Propithecus
diadema diadema and Indri indri. I continue to enjoy all our fruitful discussions on
primatology despite the distance between the continents.
I would also like to thank all people who supported and accompanied my project, which has
developed more like a web than a normal straightforward dissertation. Often, during our many
discussions, I would be handed an address of who I should contact next.
In this respect I wish to thank Dr. Werner Kaumanns, who made it possible to place my first
steps into the German Primate Center (Deutsches Primatenzentrum, DPZ, Göttingen). There,
the team of Prof. Dr. Jörg Ganzhorn and Dr. Peter Kappeler had the idea for my project: the
problem of diarrhoea of lemurs in captivity, who are otherwise thriving when eating special
plant species. And I am still thankful for their hint to contact Dr. Glander and for their
invitation to their camp in Madagascar. I am obliged to Dr. Stephanie Heiduck at the library
of the DPZ in providing me with the necessary primate literature so I could spend time at
home with my children.
My thanks also go to the staff of the DULC: to Bill Hess, who helped me to get things
organised at the DULC, and my very special thanks go to Paige Vinson and Jennifer Louise
Campbell, now graded to Dr. Campbell, who gave me shelter during my first stay. I am
grateful to David Haring, who was always helpful in answering any of my queries, especially
those questions that arose once I had returned to Germany.
I am much obliged to my husband, Mathias Abhau, who is credited with unending support.
He made every endeavour to support my activities. He shared his holidays with me in
Madagascar, helped to observe the animals at the Primate Center and visited me at diverse
laboratories. He always solved my computer woes and took the children whenever I needed
time for writing. And for all those endless discussions, he granted me patience together with
the intellectual and practical support needed during such an endeavour.
During this dissertation, I found new friends who opened their doors and helped me to get
organised, including Mrs. Doris Döring, Dr. Ludger Witte, and Mr. and Mrs. Weseloh at
Göttingen. My father often repaired my car to keep me mobile, and my mother took some
time to look after my children.
Last not least I would like to thank my study animals (Propithecus verreauxi coquereli), and
it is remembering their unique beauty and nature that gave me the most unending support to
prop me up as I continued to pursue this research project. It is my hope that this dissertation
will contribute to a better understanding of Propithecus feeding ecology, and will serve to
improve their captive living-conditions. And lastly, I hope this research will help to protect
them in the wild, which was my initial inspiration for this study.iv Abbreviations
Abbreviations
abbr. abbreviation, abbreviated
amu atomic mass units
animal groups: M&T Marcella and Tiberius
D&V Drusilla and Valentinian
J&D Julian and Drusilla
G Gordian
br. broad
BSTFA N,O-bis[trimethylsilyl]trifluoroacetamide
cAMP cyclic adenosine monophosphate
CI chemical ionisation
conc. concentrated
COSY correlation spectroscopy
d doublet
DAB Deutsches Arzneibuch (German Pharmacopoeia)
DAC Deutscher Arzneimittel Codex (German Drug Codex)
DCI-MS direct chemical ionisation mass spectrometry
dd doublet of doublets
DEPT distortionless enhancement by polarization transfer
dest. destillata
DGE Deutsche Gesellschaft für Ernährung (German society for nutrition)
dHex deoxyhexose
dHex-ol deoxyhexitol
Diast. diastereoisomer
DMSO dimethylsulfoxid
DULC Duke University Lemur Center, previously known as Duke University
Primate Center
EI-MS electron impact ionisation mass spectrometry
ESI-MS electrospray ionisation mass spectrometry
FAB-MS fast atom bombardment mass spectrometry
Gal, gal galactose
GalA galacturonic acid
GBF Gesellschaft für biotechnologische Forschung, Braunschweig
GC gas chromatography
HAB Homöopathisches Arzneibuch (Homeopathic Pharmacopoeia)
Hex hexose (aldohexose)
HexA hexuronic acidAbbreviations v
Hex-ol hexitol
HMBC heteronuclear multiple bond correlation
HPLC high pressure liquid chromatography
distance between starting line and spot
hRf 100 distance between starting line and front
HR-MS high resolution mass spectrometry
HSQC heteronuclear single quantum correlation
Hz Hertz
ID identification number
IPB Leibniz-Institut für Pflanzenbiochemie, Halle / Saale
J values for coupling constants
K-gal-rha kaempferol-3-O-α-L-rhamnopyranosyl(1→2) ß-D-galactopyranoside
K-rha kaempferol-3-O-α-L-rhamnopyranoside
LC-MS liquid chromatography mass spectrometry
m mass
M analyt molecule (mass spectrometry)
MHH Medizinische Hochschule, Hanover
min. minute
MS mass spectrometry
MSTFA N-methyl-N-(trimethylsilyl)-2,2,2-trifluoroacetamide
MTBSTFA N-methyl-N-[tert-butyldimethyl-silyl]trifluoroacetamide
MW molecular weight
n.d. not detected
NDF neutral detergent fibre
NHE natural habitat enclosure
NMR nuclear magnetic resonance
No., no. number
ÖAB Österreichisches Arzneibuch (Austrian Pharmacopoeia)
o.l. older (autumn) leaves
org. organic
p.a. pro analysis
PAS periodic acid-Schiff reagent
Ph.Eur. Pharmacopoeia Europaea
Ph.Helv. Pharmacopoeia Helvetica
prob. probability
q quartet
Q-gal-rha quercetin-3-O-α-L-rhamnopyranosyl(1→2)ß-D-galactopyranoside
q.s. (lat.) quantum satis
QZ “Quellungszahl”, swelling number
r regression coefficients
RDA retro-Diels-Alder reaction
Ref. referencevi Abbreviations
ret. retention
Rha, rha rhamnose
resp. respectively
rpm rotations per minute
s singlet
sh shoulder
t triplet
TFA trifluoroacetic acid
TLC thin layer chromatography
TMS tetramethylsilan
trace am. trace amounts
u units
USP United States Pharmacopoeia
v volume
v.br. very broad
veg. vegetables
WHO World Health Organization (Report on Infectious Diseases, 1999 & 2000)
xyl xylose
y.l. younger (autumn) leaves