Stiftung Tierärztliche Hochschule Hannover Die ontogenetische ...

Stiftung Tierärztliche Hochschule Hannover
Die ontogenetische Entwicklung des Bewegungsapparates beim Beagle – eine
morphometrische und kinetische Analyse
INAUGURAL – DISSERTATION
zur Erlangung des Grades einer Doktorin der Veterinärmedizin
- Doctor medicinae veterinariae -
(Dr. med. vet.)
vorgelegt von
Daniela Helmsmüller
Bremen
Hannover 2013

Wissenschaftliche Betreuung:
1. Prof. Dr. Ingo Nolte
Klinik für Kleintiere
2. PD Dr. Nadja Schilling
Institut für Spezielle Zoologie und
Evolutionsbiologie, Jena
1. Gutachter: Prof. Dr. Ingo Nolte
2. Gutachter: Prof. Dr. Hagen Gasse
Tag der mündlichen Prüfung: 22.5.2013
Diese Arbeit wurde im Rahmen des Kompetenzzentrum für Interdisziplinäre
Prävention (KIP) der Friedrich-Schiller-Universität Jena und der Berufsgenossenschaft
Nahrungsmittel und Gastgewerbe (BGN), Erfurt sowie durch die Hannoversche
Gesellschaft zur Förderung der Kleintiermedizin (HGFK) gefördert.

Meiner Familie und Sammy

Teile dieser Arbeit sind bei folgenden Fachzeitschriften eingereicht:
• BMC Veterinary Research
Ontogenetic allometry of the Beagle
Daniela Helmsmüller, Patrick Wefstaedt, Ingo Nolte, Nadja Schilling
• Journal of Experimental Zoology Part A
Shift of the whole-body center of mass in growing dogs
Daniela Helmsmüller, Alexandra Anders, Ingo Nolte, Nadja Schilling

Ergebnisse dieser Dissertation wurden als Poster auf folgenden Fachtagungen bzw.
als populärwissenschaftliche Artikel präsentiert:
• 18. Erfurter Tage 2011
Untersuchung der Bewegungsentwicklung beim Beagle
• Kongress der Society for Integrative and Comparative Biology 2012
Kinematic, kinetic and electromyographic analysis of the locomotor ontogeny
of the Beagle
• Kongress Canine and Equine Locomotion 2012
Locomotor ontogeny of the Beagle
• Unser Rassehund 10/2012
Vom tapsigen Welpen zum erwachsenen Hund- Untersuchung zur Entwicklung
von Körperbau und Fortbewegung am Beispiel des Beagles
• 19. Erfurter Tage 2012
Die ontogenetische Entwicklung der Fortbewegung des Beagles
• 21. Jahrestagung der Fachgruppe „Innere Medizin und klinische Labordiagnostik“
der DVG 2013
Das Wachstum mit Blick auf die Bewegung von Beaglen

Inhaltsverzeichnis
Inhaltsverzeichnis
1. Einleitung und Literaturüberblick .................................................................... 9
2. Material und Methoden ................................................................................... 12
2.1. Hunde ........................................................................................................ 12
2.2. Morphometrie............................................................................................. 13
2.3. Ganganalyse.............................................................................................. 15
3. Studie I: Ontogenetic allometry of the Beagle .............................................. 18
3.1. Abstract...................................................................................................... 18
3.2. Background................................................................................................ 19
3.3. Materials and Methods............................................................................... 22
3.4. Results....................................................................................................... 24
3.5. Discussion.................................................................................................. 27
3.6. Conclusions ............................................................................................... 32
3.7. List of abbreviations ................................................................................... 32
3.8. Competing interests ................................................................................... 33
3.9. Author contributions ................................................................................... 33
3.10. Acknowledgements.................................................................................... 33
3.11. References................................................................................................. 34
3.12. Figures....................................................................................................... 39
3.13. Tables ........................................................................................................ 44
4. Studie II: Shift of the whole-body center of mass in growing dogs............ 50
4.1. Abstract...................................................................................................... 50
4.2. Abbreviations ............................................................................................. 51
4.3. Introduction ................................................................................................ 52
4.4. Animals and Methods ................................................................................ 54
4.5. Results....................................................................................................... 56
4.6. Discussion.................................................................................................. 58
4.7. Acknowledgments...................................................................................... 61
4.8. Conflict of interest statement...................................................................... 61
4.9. Literature cited ........................................................................................... 62
4.10. Figures....................................................................................................... 67
4.11. Tables ........................................................................................................ 69
5. Diskussion ....................................................................................................... 72
6. Zusammenfassung.......................................................................................... 78
7. Summary.......................................................................................................... 80
8. Literaturverzeichnis ........................................................................................ 82
9. Danksagung..................................................................................................... 97

Abkürzungsverzeichnis
Abkürzungsverzeichnis
Br
Cr
CoM
D
Fe
Fz
PW
Sk
Brachium
Crus
Körpermasseschwerpunkt
Duty Factor
Femur
vertikale Kraft
postnatale Woche
Skapula

Einleitung und Literaturüberblick
1. Einleitung und Literaturüberblick
Hunde gehören wie ihre Vorfahren, die Wölfe, zu den sogenannten cursorialen
Säugetieren, die an das Zurücklegen großer Strecken bei relativ hoher Fortbewegungsgeschwindigkeit
angepasst sind (LULL 1904; GREGORY 1912). Dafür ist ein
gesundes, normal entwickeltes muskulo-skelettales System eine essenzielle
Voraussetzung.
Aufgrund von alimentären Mängeln oder auch durch pathologische Prozesse,
Infektionen, Traumata oder genetische Einflüsse kann es in der besonders sensiblen
Phase des Wachstums zu Störungen in der Entwicklung des Bewegungsapparates
kommen. Auch der Besitzerwechsel, zumeist zwischen der 9ten und 12ten
Lebenswoche, kann durch sozialen Stress und Veränderungen der Lebensweise
Wachstumsstörungen provozieren. Für eine Beurteilung des physiologischen
Wachstums- und Entwicklungszustandes des Bewegungsapparates von jungen
Hunden, aber auch für Verlaufskontrollen therapeutischer und rehabilitativer
Maßnahmen ist es daher unerlässlich, die genauen zeitlichen Charakteristika der
Ontogenese des Bewegungsapparates von Hunden zu kennen und Referenzdaten
der physiologischen Entwicklung verfügbar zu haben.
Wie andere junge Säugetiere sind auch junge Hunde nicht einfach kleine Kopien
der Adulti, sondern sie unterscheiden sich deutlich in zahlreichen physiologischen
und morphometrischen Parametern. Zum Beispiel erreichen junge kalifornische
Eselhasen höhere relative Beschleunigungen als die Adulti durch günstigere
Hebelarmverhältnisse und eine größere Krafterzeugung der Muskulatur bezogen auf
die Körpermasse (CARRIER 1983). Fohlen sparen metabolische Energie auf den
langen Wanderungen ihrer Herden, indem sie bezogen auf ihre Beinlänge relativ
größere Schritte machen (GROSSI u. CANALS 2010). Solche biomechanischen
Vorteile erlauben es jungen Säugetieren, in der gleichen Umwelt und unter den
gleichen Bedingungen, z.B. in Bezug auf die Nahrungssuche oder natürliche Feinde,
wie die Adulti zu überleben. Bei Wölfen oder Wildhunden sind keine Studien über
solche physiologischen Veränderungen in der Ontogenese bekannt.
Bezüglich morphometrischer Unterschiede zwischen juvenilen und adulten
Vertretern der Säugetiere ist allgemein bekannt, dass Jungtiere einen großen Kopf
9

Einleitung und Literaturüberblick
und große Autopodien im Vergleich zu den adulten Proportionen haben. Im Verlauf
der Entwicklung wachsen beide Körperteile weniger, verglichen mit anderen
Körperabschnitten oder auch der Körpergröße. Solche morphometrischen
Veränderungen wirken sich auf die Verteilung des Körpergewichtes innerhalb und
zwischen den Extremitäten und damit auf die relative Lage des Körpermasseschwerpunktes
aus (KIMURA 1987, 2000; YOUNG 2012). Interspezifische Vergleiche
adulter Säugetiere belegen beispielsweise, dass der Gepard aufgrund seiner
muskulösen Hinterbeine 52% seines Körpergewichtes auf den Vorderextremitäten
trägt, während das Kamel mit seinem muskulöseren Vorderkörper 66% der
Körpermasse durch die Vorderbeine unterstützt (ROLLINSON u. MARTIN 1981).
Intraspezifische Unterschiede wurden bei Pferden zwischen Warmblütern, die mehr
Gewicht auf den Vorderbeinen tragen, und dem American Quarter Horse beobachtet
(BACK et al. 2007). Auch bei Hunden lassen sich rassetypische Unterschiede
erkennen. Der Barsoi, ein Windhund mit kräftigen Hinterbeinen, trägt 57%, der
Rottweiler, als Molosser, trägt 64% des Körpergewichts auf den Vorderbeinen
(BERTRAM et al. 2000; WILLIAMS et al. 2008; VOSS et al. 2011).
Ontogenetisch wurde der Einfluss der Verschiebungen der Körperproportionen auf
die Lage des Körpermasseschwerpunktes bisher nur für Primaten untersucht. Hier
wurde übereinstimmend eine Verschiebung nach caudal beobachtet, da die meisten
Primaten als Adulti den größeren Teil ihres Körpergewichtes auf den muskulöseren
Hinterbeinen tragen (GRAND 1977; TURNQUIST u. WELLS 1994;
KIMURA 1987, 2000; SHAPIRO u. RAICHLEN 2006; YOUNG 2012). Ob sich der
Körpermasseschwerpunkt bei Säugetieren, die als Adulti über 50% ihres Körpergewichts
auf den Vorderbeinen tragen (wie z.B. Hunde), während der Ontogenese auch
von cranial nach caudal verschiebt oder eine Akzentuierung des ohnehin cranial
liegenden Schwerpunktes erfolgt, wurde bisher nicht detailliert untersucht.
Wenige Studien haben sich in der Vergangenheit mit den physiologischen
Veränderungen und dem relativen Wachstum der Körperabschnitte, der sogenannten
ontogenetischen Allometrie, während des postnatalen Wachstums des Hundes
beschäftigt. WEISE (1964) und SCHULZE et al. (2003, 2007) beobachteten, dass
Größenunterschiede zwischen den verschiedenen Rassen nicht aufgrund
10

Einleitung und Literaturüberblick
unterschiedlicher Wachstumsdauer, sondern durch unterschiedlich intensives
Wachstum auftreten. WEISE (1964) untersuchte dafür vergleichend das Knochenwachstum
jeweils eines Wurfes von acht verschiedenen Rassen zwischen dem
30ten und 120ten Lebenstag. Somit endet ihre Studie ungefähr zu dem Zeitpunkt, an
dem Junghunde an ihre neuen Besitzer übergeben werden. SCHULZE et al. (2003,
2007) untersuchten das Knochenwachstum der Vorder- und Hintergliedmaßen bei
vier Rassen. Sie beobachteten den Abschluss des Wachstums z.B. beim Beagle um
den 305ten Tag. Das Skelettwachstum und die Entwicklung der Körpermasse
wurden ebenfalls von SALOMON et al. (1999) beim Beagle untersucht.
Keine der oben genannten Studien schloss die Skapula als lokomotorisch
wichtigen Abschnitt der Vorderextremität ein. Dieser proximale Abschnitt der
Vordergliedmaße trägt durch seinen hoch gelegenen Drehpunkt maßgeblich zum
Vortrieb des Körpers während der Fortbewegung bei; allein zwischen 65% und 80%
der Schrittlänge sind auf die Bewegungen der Skapula zurückzuführen (FISCHER u.
LILJE 2011). Durch den allein sehnigen und muskulösen Verbund der Vordergliedmaße
mit dem Rumpf dient sie auch dem Auffangen der Last im Stand, in der
Bewegung und beim Sprung. Während der Evolution der Säugetiere wurde die
Skapula aus dem ursprünglich starren Schultergürtel gelöst und in die bewegliche
Kette der Vordergliedmaßensegmente integriert (FISCHER 1998). Damit verbunden
löst sich die ursprüngliche serielle Homologie der Extremitätenabschnitte der
tetrapoden Vorder- und Hintergliedmaßen mit den homologen Elementen des
Stylopodiums (Humerus, Femur), des Zeugopodiums (Radius, Tibia; Ulna, Fibula)
und des Autopodiums (Carpus, Tarsus; Metacarpus, Metatarsus; Phalanges) auf. Sie
wird bei den Theria durch eine neue funktionelle Homologie der Extremitätenabschnitte,
begründet auf deren Bewegungstrajektorien und Drehpunktshöhen,
ersetzt. Funktionell entsprechen sich bei diesen Säugetieren wie auch beim Hund:
Skapula und Femur, Brachium und Crus und Antebrachium und Tarsus.
Weiterhin wurden wachsende Hunde bisher lokomotorisch nur in einer Studie
untersucht, die allerdings nicht vollständig, sondern nur als Zusammenfassung,
publiziert wurde (BIKNEVICIUS et al. 1997).
11

Material und Methoden
Ziel dieser Arbeit war die detaillierte Beschreibung der allometrischen Veränderungen
aller Extremitäten- und Körperabschnitte während der Entwicklung von
Beaglen und die Untersuchung der Auswirkungen dieser Veränderungen auf die
kraniokaudale Lage des Körpermasseschwerpunktes. Im Fokus der Arbeit stand die
Erhebung von Referenzdaten für die physiologische Entwicklung des Bewegungsapparates.
Diese Studie wurde am Beispiel des Beagles durchgeführt, weil er als
mittelgroße Rasse der Laufhunde einen Vergleich mit bereits publizierten Daten zu
Hunden mit anderen Körperformen und -größen erlaubt. Darüber hinaus ist der
Beagle ein typischer Laborhund. Hunde variieren wie keine andere Säugetierart in
Körpergröße und Gestalt (FISCHER u. LILJE 2011), daher ist die Kenntnis von
möglichen Unterschieden im Wachstum von Bedeutung. Die vorgelegte Arbeit soll
hierzu durch die detaillierte Untersuchung einer Rasse einen Beitrag leisten.
Die Ergebnisse dieser Arbeit werden in zwei getrennten Studien präsentiert, um
eine ausführliche Einordnung der einzelnen Befunde in die vorhandene Datenlage
und die entsprechende Diskussion dieser zu ermöglichen. Dabei werden in der
ersten Studie die in dieser Arbeit erhobenen morphometrischen Daten vorgestellt. Es
erfolgt ein Vergleich mit Daten aus vorherigen Studien über andere Beaglelinien und
Hunderassen und eine Einordnung innerhalb der Säugetiergruppe. Die zweite Studie
umfasst die kinetischen Daten und untersucht die Lage des Körpermasseschwerpunktes
während der Ontogenese. Die Ergebnisse werden mit Blick auf anatomische
Veränderungen diskutiert und mit Ergebnissen von anderen Säugetieren verglichen.
2. Material und Methoden
2.1. Hunde
Diese Studie wurde anhand von sechs Beaglerüden durchgeführt. Diese stammten
aus einem Wurf (Größe: 7 männliche, 4 weibliche) aus der Reproduktionsmedizinischen
Einheit der Stiftung Tierärztliche Hochschule Hannover und kamen im Alter
von neun Wochen in die Klinik für Kleintiere derselben Hochschule. Hier wurden die
Junghunde unter den gleichen Bedingungen in einer Gruppe gehalten.
Die Messungen begannen mit Ankunft der Junghunde in der Klinik für Kleintiere
mit neun Wochen und endeten mit einem Alter der Hunde von 51 Wochen. Bis zum
12

Material und Methoden
Alter von 20 Wochen wurden die Daten wöchentlich, bis 32 Wochen alle zwei
Wochen und anschließend monatlich bis zum Ende der Studie erhoben.
Mit einem Alter von neun und zwölf Wochen wurden alle Hunde gegen Staupe,
Parvovirose, Hepatitis contagiosa canis, Leptospirose und Tollwut geimpft. Trotzdem
erkrankten die Hunde zwischen der 15ten und 19ten Lebenswoche an Parvovirose,
so dass in diesen Wochen keine Messungen stattfinden konnten. Während des
Jahres, in dem mit den Hunden gearbeitet wurden, befand sich ihr Body Condition
Score innerhalb der normalen Bandbreite zwischen vier und sechs, eingestuft nach
dem Body Condition Score System des Nestlé Purina Pet Care Centre (St. Louis,
MO, USA) mit Werten von eins bis neun (1-3 zu dünn, 4-5 ideal, 6-9 zu dick).
In der 14ten und der 50ten Lebenswoche wurden die Junghunde orthopädisch
untersucht, wobei kein besonderer Befund festgestellt wurde.
2.2. Morphometrie
Kopf- und Rumpflänge, Widerrist- und Beckenhöhe sowie Brustkorbumfang,
Beckenlänge und die Länge der einzelnen Gliedmaßenabschnitte wurden anhand
von palpierbaren Knochenpunkten mit einem konventionellen Maßband (Genauigkeit:
5 mm) an der linken Körperseite gemessen (Abb. 1, Studie 1). Die verwendeten
anatomischen Landmarken sind in Tabelle 1 aufgeführt. In Abweichung zu
klassischen anatomischen Messstrecken wurden in dieser Arbeit bewußt funktionell,
für die Lokomotion relevante Strecken vermessen. So entspricht beispielsweise
Strecke 10 der funktionellen Rumpflänge, d.h. der Strecken zwischen den
Drehpunkten der Vorder- und der Hinterextremität. Die Strecken entlang der Vorderbzw.
Hinterextremität sind an die Längen zwischen Drehpunkten der Gelenke
angelehnt (Schilling & Petrovitch 2006). Darüber hinaus mußten nicht zuletzt auch
Landmarken ausgewählt werden, die an allen Hunden unabhängig vom Alter
eindeutig ansprechbar sind und zu reproduzierbaren Längenmessungen führen. Das
Körpergewicht wurde mit einer Waage bis zur ersten Dezimalstelle gemessen. Zum
Vergleich wurden auch die Elterntiere vermessen, zu diesem Zeitpunkt waren die
Junghunde 32 Wochen alt.
13

Material und Methoden
Wachstumskurven für die Gewichtsentwicklung und die Entwicklung der mittleren
Werte der Gliedmaßensegmente wurden mit Hilfe der Gompertzfunktion nach
HELMINK et al. (2000) berechnet:
(1) m t =m max exp(-e [-(t-c)/b] )
wobei m t Masse zum Zeitpunkt t, m max geschätztes Endgewicht, b proportional zur
Wachstumsdauer und c das Alter im Wendepunkt (hier 36,8% des Endgewichtes) ist.
Alle morphometrischen Daten wurden doppeltlogarithmisch gegen die Körpermasse
aufgetragen. Anschließend wurde die Regressionsgerade mit Hilfe des Modells II der
RMA (reduced major axis regression) berechnet. Dazu diente die logarithmierte
Allometriegleichung
(2) logy= b logx + loga.
y stellte dabei die Körperteilgröße dar, x die Bezugsgröße wie z.B. die Körpergröße
oder die Körpermasse, a ist die Integrationskonstante für weitere Einflüsse und b
der allometrische Koeffizient, der die Steigung der Geraden und somit den Anteil von
y an x bestimmt. Werden Größen derselben Dimension verglichen (z.B. zwei
Strecken zueinander), verhalten diese sich isometrisch bei b=1,00, positiv
allometrisch bei b>1,00 und negativ allometrisch bei b

Material und Methoden
Körpermaß
Messstrecke
Becken Strecke 5 Tuber coxae – Tuber ischiadicum
Strecke 6 Trochanter major - Condylus lateralis femoris
Hintergliedmaße
Strecke 7 Condylus lateralis femoris - Malleolus lateralis
Malleolus lateralis - Distal dritte Zehe (mit
Strecke 8
aufgenommener Pfote)
Strecke 9 Auf Höhe des Processus xyphoideus
Körperproportionen
Trochanter major
Cranialer Rand der Skapula waagerecht bis zum
Strecke 10
Strecke 11 Nasenspiegel – Protuberantia occipitalis externa
2.3. Ganganalyse
Im Rahmen der instrumentierten Ganganalyse werden die Parameter Bodenreaktionskraft,
Gelenk- und Segmentwinkel und zeitliche Gangcharakteristika analysiert.
Die ganganalytischen Untersuchungen in dieser Studie wurden in dem Labor der
Klinik für Kleintiere auf einem Laufband mit je einer Kraftmessplatte unter den vier
separaten Riemen (Modell 4060-08, Bertec Corporation, Columbus, OH, USA) im
Schritt und im Trab durchgeführt. Pro Geschwindigkeit erfolgten wenigstens 3
Aufnahmen mit einer jeweiligen Dauer von ca. 30 Sekunden (ca. 65 Schritte). Die
Aufzeichnung der Daten erfolgte mit Vicon Nexus (Vicon Motion System Ltd., Oxford,
UK). Während der Messungen auf dem Laufband wurden für kinematische
Untersuchungen insgesamt 25 retroreflexive Marker an palpierbare Knochenpunkte
geklebt. Weiterhin wurde unter Verwendung von Oberflächenelektromyographie die
Aktivität des M. longissimus thoracis et lumborum bilateral während des Laufens auf
dem Laufband gemessen. Der Fokus der Auswertungen dieser Arbeit liegt dabei auf
den kinetischen Daten.
Die Messung der Bodenreaktionskräfte in den drei Richtungen des Koordinatensystems
(x, y, z) erfolgte während des Laufens auf dem Laufband. Am Verhältnis
zwischen den vertikalen Bodenreaktionskräften (Fz) der Vorder- und der Hintergliedmaßen
kann die kraniokaudale Lage des Körpermasseschwerpunktes (CoM)
abgeschätzt werden. Des Weiteren hat LEE et al. (2004) durch eine experimentelle
Verschiebung des CoM durch Erhöhung des Gewichts entweder auf den Vorderoder
den Hintergliedmaßen beim Hund gezeigt, dass sich diese Veränderungen auch
auf das Verhältnis der Stemmphasendauer der Gliedmaßen auswirken. Daher lag in
15

Material und Methoden
dieser Studie der Fokus auf der Auswertung der vertikalen Kräfte (maximale Kraft,
mittlere Kraft, Impuls) und des Verhältnisses der Stemmphasendauer der Vorderund
Hintergliedmaßen. Weiterführend wurde ein Symmetrieindex zur Überprüfung
der Lahmheitsfreiheit und die Zeit bis zum Auftreten der maximalen vertikalen Kraft
bestimmt.
Aufgrund ihrer geringen Körpergröße liefen die Hunde nur auf einer Seite des
Laufbandes. Dadurch wurden nur die Kräfte der Vorder- und Hintergliedmaßen
getrennt aufgenommen und nicht einer jeden einzelnen Gliedmaße. Trotzdem
konnten im Trab durch die gemeinsame Flugphase der Vorder- bzw. Hinterextremitäten
und dem damit verbundenen Duty Factor von D

Material und Methoden
Körpergewicht des Hundes normiert. Aus diesen Daten wurden die maximale und die
mittlere vertikalen Bodenreaktionskraft sowie der vertikale Impuls ermittelt. Alle
Ergebnisse wurden statistisch mit dem Programm GraphPad Prism (Version 4,
GraphPad Software, Inc. California Corporation, CA, USA) bewertet.
17

Studie I: Ontogenetic allometry of the Beagle
Studie I: Ontogenetic allometry of the Beagle
Daniela Helmsmüller 1
daniela.helmsmueller@tiho-hannover.de
Patrick Wefstaedt 1
patrick.wefstaedt@tiho-hannover.de
Ingo Nolte 1
ingo.nolte@tiho-hannover.de
Nadja Schilling 1,2*
nadja.schilling@tiho-hannover.de
1 Small Animal Clinic, University of Veterinary Medicine Hannover, Foundation,
Bünteweg 9, 30559 Hannover, Germany
2 Institute of Systematic Zoology and Evolutionary Biology, Friedrich-Schiller-
University, Erbertstr. 1, 07743 Jena, Germany
*Corresponding author
2.4. Abstract
Background: Mammalian juveniles undergo dramatic changes in body conformation
during development. As one of the most common companion animals, the time
line and trajectory of a dog’s development and its body’s re-proportioning is of
particular scientific interest. Several ontogenetic studies have investigated the
skeletal development in dogs, but none has paid heed to the scapula as a critical part
of the mammalian forelimb. Its functional integration into the forelimb changed the
correspondence between fore- and hindlimb segments and previous ontogenetic
studies observed more similar growth patterns for functionally than serially
homologous elements. In this study, the ontogenetic development of six Beagle
18

Studie I: Ontogenetic allometry of the Beagle
siblings was monitored between 9 and 51 weeks of age to investigate their skeletal
allometry and compare this with data from other lines, breeds and species.
Results: Body mass increased exponentially with time; log linear increase was
observed up to the age of 15 weeks. Compared with body mass, withers and pelvic
height as well as the lengths of the trunk, scapula, brachium and antebrachium,
femur and crus exhibited positive allometry. Trunk circumference and pes showed
negative allometry in all, pelvis and manus in most dogs. Thus, the typical
mammalian intralimb re-proportioning with the proximal limb elements exhibiting
positive allometry and the very distal ones showing negative allometry was observed.
Relative lengths of the antebrachium, femur and crus increased, while those of the
distal elements decreased.
Conclusions: Beagles are fully-grown regarding body height but not body mass at
about one year of age. Particular attention should be paid to feeding and physical
exertion during the first 15 weeks when they grow more intensively. Compared with
its siblings, a puppy’s size at 9 weeks is a good indicator for its final size. Among
siblings, growth duration may vary substantially and appears not to be related to the
adult size. Within breeds, a longer time to physically mature is hypothesized for
larger-bodied breeding lines. Similar to other mammals, the Beagle displayed nearly
optimal intralimb proportions throughout development. Neither the forelimbs nor the
hindlimbs conformed with the previously observed pattern of a proximo-distal growth
gradient. Potential factors responsible for variations in the ontogenetic allometry of
mammals need further evaluation.
Keywords: Scaling, limb proportions, body proportions, bone growth, serial
homology, body mass
2.5. Background
The physical development from a puppy to an adult dog is characterized by
dramatic changes in body size and shape. Mammalian juveniles in general are not
simply small copies of adults; they differ substantially in their body proportions and
often appear clumsy in their movements (e.g., [1-3]). The juvenile body grows
19

Studie I: Ontogenetic allometry of the Beagle
continuously while the musculoskeletal and nervous systems progressively mature.
At the same time, juveniles have to perform in the same environment as adults,
which results in unique challenges due to the differences in body size and
conformation [4].
As the dog is one of the most common companion animals, the timeline and
trajectories of its postnatal re-proportioning as well as the age at which it reaches
adult proportions are of particular interest. Puppies are usually acquired by their new
owners at the age of 9 to 11 weeks. For both the breeder and the potential buyer, the
prospective physical development may be relevant when selecting a puppy.
However, at the referral, the dogs are obviously not fully grown. Furthermore, during
postnatal development, growth problems due to diet, injury or illness may occur and it
is important to have reference values for the postnatal growth of the various body
parts. A number of allometric studies are available for adult dogs; for example,
comparing different breeds or examining historical or genetic transformations (e.g.,
[5-12]). Of the ontogenetic studies, some focused on pathological processes (e.g.,
[13,14]), while others documented either the physiological and pathological
development of a single limb segment (e.g., [15-17]) or of several body parts [18-23].
Using x-ray in a longitudinal approach, Yonamine et al. [19] and Conzemius et al.
[20] examined the growth of the forelimb or a part of it, respectively. Weise [18]
followed the changes in body proportions among siblings in eight breeds and
concluded that size differences among siblings are not due to differences in the
duration of growth but growth rate. Schulze and colleagues [22,23] studied four
breeds and a greater number of individuals per breed compared to Weise [18];
similarly, they observed that larger breeds differ from smaller breeds in their growth
rates rather than growth duration. Salomon et al. [21] monitored 14 measurements of
37 Beagles during the first 13 months. They observed a higher growth rate in the
hindlimbs than the forelimbs and no sex difference in growth termination. In contrast
to the studies mentioned above [22,23] and in accordance with Hawthorne et al. [24],
who investigated body mass development in different breeds, Salomon et al. [21]
concluded that larger breeds grow for a longer time.
20

Studie I: Ontogenetic allometry of the Beagle
To investigate the ontogenetic scaling in dogs, this study monitored the allometry
in Beagle siblings. The Beagle is a British breed and belongs to the hound group
within the sporting breeds and has been bred for pack hunting hares and rabbits.
Nowadays, the Beagle is also a very popular family dog and a common laboratory
animal. Within the breed, lines with different body sizes and proportions have been
bred. Previous ontogenetic studies on Beagles worked with relatively small- to
medium-sized lines (e.g., [19] adult body mass ca. 10 kg; [21] ca. 11 kg; [24] ca. 17
kg). In the current study, juveniles of a relatively large-bodied line were used (adult
mass ca. 21 kg), allowing for a comparison of growth patterns among different-sized
lines of the same breed.
During the evolution of mammals, fore- and hindlimbs underwent a profound
reorganization that accompanied the transformation from a sprawled to a parasagittal
limb posture. This resulted in a dissociation between serially and functionally
homologous elements in the limbs (reviewed in [25]). The scapula was mobilized and
is functionally analogous to the femur in mammals [26,27]. As a result, both fore- and
hindlimbs can be described as three-segmented limbs arranged in a zig-zagconfiguration
with the most proximal elements (i.e., scapula, femur), the middle
segment (i.e., brachium, crus) and the distal segments (antebrachium, pes) being
functionally analogous due to their similar direction and amplitude of motion. Only a
few allometric studies on adult (e.g., [25,28]) and juvenile mammals (e.g., [29-32])
paid heed to this evolutionarily ‘new’ functional homology of the limb segments by
taking the scapula into account. Comparing the results of these studies showed that
in small mammals with a crouched limb posture the functionally homologous
segments resemble each other more in their growth pattern than the serially
homologous elements [32]. Three principles were proposed based on these data:
First, the functionally homologous limb segments show more similar allometric
coefficients than the serially homologous elements. Second, the limbs show a
proximo-distal gradient in their growth with the proximal segment growing the most
and the distal segment growing the least. Third, the middle segment (i.e., brachium
and crus) remains nearly constant in its proportion of the limb’s anatomical length.
21

Studie I: Ontogenetic allometry of the Beagle
Unfortunately, no ontogenetic study in dogs included the scapula in their measurements,
hindering testing the proposed ontogenetic principles in dogs.
The aims of this study were 1) to test the observation that small and large dogs
differ in rate but not duration of growth at the level of siblings, lines and breeds and 2)
to examine the ontogenetic scaling of the Beagle in the light of the ontogenetic
principles observed in other mammals.
2.6. Materials and Methods
Dogs
Six male Beagle siblings from the same litter (litter size: 7 males, 4 females) were
used in this longitudinal study. The dogs were from a breeding colony of the
University of Veterinary Medicine Hannover (Germany) and came to the Small
Animal Clinic at the age of 9 weeks. One male and all females remained in the
breeding colony and were not enrolled in this study to ensure similar husbandry
conditions for the dogs investigated. All experiments were carried out in strict
accordance with German Animal Welfare Regulations and were approved by the
Ethics Committee of Lower Saxony, Germany.
Measuring started at 9 weeks and continued until the dogs were 51 weeks old.
Data were collected weekly up to the age of 20 weeks, fortnightly up to 32 weeks and
monthly till the end of the study. After that, only body mass was determined again at
the age of 60 weeks. The dogs were kept and raised together in a group and under
the same conditions, regarding, for example diet and exercise. Only one dog (#4)
had to be regrouped at the age of 33 weeks, but its dietary plan and physical activity
was comparable to that of its siblings. All dogs were vaccinated against distemper,
hepatitis, canine parvovirus, leptospirosis and rabies at 9 and 12 weeks. However,
between the age of 15 and 19 weeks, the dogs suffered from canine parvovirus and
no measurements could be taken during this period. All puppies primarily experienced
gastrointestinal upset and were treated immediately and aggressively in our
clinics (i.e., fluid replacement, dietary restrictions, antiemetic and antibiotic therapy).
As cell turnover in the gastrointestinal tract is rapid (1-3 days), intestinal malabsorption
is short-lived and recovery from this enteric form is rapid [33].
22

Studie I: Ontogenetic allometry of the Beagle
At the age of about 40 weeks, all dogs were neutered. Between 32 and 51 weeks,
occasionally smaller infections or injuries prevented the data collection from one or
the other dog. During the study period, all dogs underwent two standard orthopedic
investigations, one at 14 and one at 50 weeks of age, which confirmed that the dogs
were healthy. The dogs were fed three times a day till the age of 44 weeks,
afterwards twice a day. Portion size was about 1.9% of the dog’s body mass. At
about 50 weeks, adult feed replaced the puppy feed. Over the course of the year
when the dogs were investigated, their body index was in the normal range between
4 and 6 based on the body condition score (Nestlé Purina Pet Care Centre, St. Louis,
MO, USA), in which values range from 1 to 9 (1-3 too thin; 4-5 ideal, 6-9 too heavy).
For comparison, the parents were also measured when their offspring were about 32
weeks old. At this time, the sire was 7 years old and had a score of 7 and the dam
was 6 years and had a score of 6.
Data collection and analyses
Body mass was determined to the first decimal using a traditional scale. A growth
curve was constructed by plotting body mass against age using the Gompertz
equation in the form: mt= mmaxexp(-exp[-(t-c)/b]), where mt is mass at time t, mmax
is mature body mass, b is proportional to duration of growth, c is the age at point of
inflection (i.e., 36.8% of mature body mass) and t is age in weeks (for details, see
[34]). Growth duration to reach 98% of the mature body mass was estimated as
4b+c. Similarly, 50% of growth duration was determined as 0.37b+c and 95% as
3b+c. All parameters were calculated for each dog and for the mean values for all
dogs using a nonlinear regression program (NLREG; www.nlreg.com).
The lengths of the head, trunk and limb segments, trunk circumference as well as
withers and pelvic heights were measured on the left body side using palpable
skeletal landmarks and a traditional measuring tape (accuracy 5 mm, Figure 1). To
reduce measurement errors, the measurements were always carried out by the same
experienced experimenter (NS) and repeated three times per measurement. From
these, means and the anatomical limb length (i.e., sum of the lengths of all
segments) were calculated for further analysis. Correlation between the proportion of
23

Studie I: Ontogenetic allometry of the Beagle
a respective segment of the anatomical limb length and age was calculated and
tested for significance. To compare our results with previous findings [21], the
Gompertz equation was also used to calculate the age when 95% of the final length
of the brachium, antebrachium, femur and crus were reached.
Data analysis followed previous ontogenetic analyses [32,35]. For the allometric
comparisons, the data were plotted on log-log scales (base 10) and regression lines
were calculated by model II of the reduced major axis regression (RMA). Model II is
to be preferred if variables, in this case body size parameters, could not be
determined without error [36]. Besides, least-squares regression can lead to biased
results if log-log bivariate regressions are used [37]. RMA regressions were
calculated using Microsoft Excel (2000). The validity of the data obtained using Excel
was previously tested and verified [32], and reevaluated for the current study using
the software RMA (v. 1.17; www.bio.sdsu.edu/pub/andy/RMA.html). The exponent
describing the slope of the regression curve is the allometric coefficient b. It indicates
whether growth is isometric, negative or positive allometric. If a one-dimensional
parameter (e.g., head length) is plotted vs. a three-dimensional one (e.g., body
mass), isometry is given by b=0.333, negative allometry by b0.333. Comparing the same dimensions (e.g., two lengths), isometry
is given by b=1.000, negative allometry by b1.000. To test
whether the allometric coefficients were significantly different from isometry, the 95%
confidence intervals surrounding the slopes were calculated. If the interval
overlapped with the slope, it was considered isometric. For comparisons among
dogs, but also with previously published data from other mammals, so-called ‘growth
sequences’ were determined by sorting the slopes from the greatest to the lowest
values. The slopes of two adjacent measurements were not considered different if
their confidence intervals overlapped.
2.7. Results
Body mass
The dogs gained weight throughout the study period (Figure 2). The fit of the
Gompertz equation to the body mass data was good (mean R2= 0.987). The
24

Studie I: Ontogenetic allometry of the Beagle
estimated mean parameters were: Mature body mass mmax=17.5±0.3kg (individual
dogs ranging between 16 kg and 20 kg), age at point of inflection c=11.1±0.3 weeks
(ranging between 10.1 and 11.2 weeks) and proportional to growth duration
b=9.18±0.7 (ranging between 8 and 10.6). On average, all dogs had reached 50% of
their mature body mass with 14.5 weeks. Until the age of 15 weeks, log body mass
increased linearly (R2=0.990). Mean age at 95% of the mature body mass was 39
weeks and at 98% 48 weeks. By the end of the study, no dog had reached the sire’s
body mass (Figure 2), but as mentioned above, he was slightly overweight.
Furthermore, dogs continue to gain muscle mass during their first years of life (see
discussion).
At week 9, dog #3 was the lightest individual (4.8 kg) and remained so until 51
weeks of age (16.1 kg). Similarly, the heaviest puppies at 9 weeks continued to be
the heaviest dogs until week 51 (#1: 6.2 kg and 20.2 kg; #5: 6.0 kg and 20.9 kg).
Interestingly, the relative body mass difference between the lightest and heaviest
sibling (ca. 22% of body mass) persisted throughout the study. Between 15 and 19
weeks, some dogs showed only very little gain in body mass; however, they returned
to their ontogenetic trajectory within a few weeks. Dog #4 did not gain any weight
during this period, being the dog most affected by the parvovirus infection. He was
back on his trajectory and among the sibling’s masses within 5 weeks after recovery.
Body proportions
Compared to body mass, withers height, pelvic height, and trunk length exhibited
positive allometry (Figure 3, Table 1).
By the end of the study, all dogs had reached at least the mean withers and pelvic
heights of the parents (46.5 cm and 43.5 cm, respectively). The only exception was
dog #3, which remained smaller (44.3 cm and 40.7 cm) and also consistently showed
the lowest values during the study. The sire’s withers and pelvic heights (48.3 cm
and 45 cm) were surpassed by the two heaviest juveniles (#1: 51.3 cm and 47.7 cm;
#5: 51.7 cm and 46.7 cm). Comparing the final heights with the values at 9 weeks
shows that dog #5 grew the least of all dogs (36.8% and 33.2% increase in withers
and pelvic height, respectively), whereas #1 grew the most as gauged by withers
25

Studie I: Ontogenetic allometry of the Beagle
height (41.9%) but was in the middle range regarding its pelvic height increase
(39.5%). Although dog #3 increased in his absolute withers height the least (17 cm),
he was in the middle range regarding his relative increase (39.1%). Dog #4, despite
suffering the most from the infection, gained the most in pelvic height of all dogs
during the course of the study (41.6%). On average, 95% of the final height was
reached at 212 days for withers height and 186 days for pelvic height.
The trunk length of the sire (47 cm) was reached or exceeded by all dogs except
#3 (43.7 cm), who also did not reach the dam’s value (45.6 cm). Dog #5 had the
longest trunk at 51 weeks (49.0 cm); he was also longer than #1 (47.8 cm), although
#1 grew absolutely (21.2 cm) and relatively (44%) the most. The lightest puppy (#3)
had the shortest trunk at 51 weeks (43.7 cm) and also grew the least during the study
period (37.4%). Trunk circumference showed negative allometry relative to body
mass for all dogs (Table 1). Mean trunk circumference of the parents was reached by
none of the juveniles during the first 51 weeks (66.8 cm); dog #5 was the one who
most closely approached that of the parents (65.3 cm).
Three dogs exhibited negative allometry regarding their head lengths relative to
body mass, dog #3 and #6 showed isometry (b=0.331 and b=0.335), and dog #1
showed positive allometry (b=0.340; Figure 3). Dog #3 (22.3 cm) and #4 (22.2 cm)
were the only ones at 51 weeks, which lagged behind when compared with the
parents’ head lengths (mean 23.3 cm). Despite having a relatively short head, #3
showed the second greatest increase in head length during the study period. In
accordance with his overall large body size, #1 was the one with the longest head
(25.5 cm). Relative to trunk length, head length exhibited negative allometry for all
dogs.
Limb proportions
Coefficients of segment lengths to body mass exhibited positive allometry for all
dogs regarding scapula, brachium, antebrachium, femur and crus (Figure 4, Table 2).
Pelvis, manus and pes showed negative allometry relative to body mass in all
dogs, except the manus in dog #6 and pes in dog #4 (Table 2). Averaged across all
individuals, the antebrachium had the highest allometric coefficient among the
26

Studie I: Ontogenetic allometry of the Beagle
forelimb segments, followed by the brachium and the scapula (Figure 3). Thus, the
growth sequence for the forelimb was ab>br=sc>ma (for individual sequences, see
Table 2). In the hindlimb, femur and crus showed no significant difference, resulting
in the growth sequence fe=cr>ps for all dogs.
Proportions of the scapula and brachium of the anatomical forelimb length
remained unchanged during development (sc: 29.0% vs. 28.1% and br: 24% vs.
24.8% at 9 and 51 weeks, respectively; Figure 5). In contrast, the antebrachium’s
proportion was significantly correlated with age and increased from 25.8% at 9 to
27.5% at 51 weeks. In the hindlimb, the relative length of both femur and crus
increased (fe: 33.8% vs. 35.9% and cr: 30.9% vs. 33.7% at 9 and 51 weeks,
respectively). The distal elements, manus and pes, were inversely correlated with
age (ma: 21.2% vs. 19.6% and pes: 35.2% vs. 30.4% at 9 and 51 weeks, respectively).
2.8. Discussion
As only male siblings were investigated in this study, no implications for sex
related differences can be drawn. However, previous studies found significant
ontogenetic differences between sexes only for large breeds like the Great Dane or
Bernese Mountain Dog but not for smaller breeds like the Beagle [19,21-23,38].
Body mass
Comparing siblings of the same litters, Weise [18] observed wide ranges in the
end dates of the growth of several skeletal parameters, indicating that the growth
duration of siblings is not related with their final size. Albeit only a fraction of the
siblings of one litter was studied herein, our findings support this observation. For
example, the lightest dog did not reach its adult mass before the heavier ones and
vice versa. Interestingly, the order among the siblings regarding body mass remained
nearly unchanged during ontogeny. The lightest puppy at 9 weeks remained the
lightest till the end of the study, and conversely, the heaviest puppies continued to be
heavy throughout the study. This was true despite some puppies being affected by
illness, because they quickly returned to their growth trajectory. Thus, our
27

Studie I: Ontogenetic allometry of the Beagle
observation confirms Weise’s remark that a puppy’s size at 9 weeks is a good
indication for its later size compared with its siblings.
Although the period of the maximal growth rate was not covered in the current
study, because maximal weight gain occurs during the first 9 to 10 weeks in Beagles
[21], log body mass still increased linearly up to the 15th week in the Beagles studied
herein. Likewise, Hawthorne and colleagues reported an exponential growth rate up
to 14 to 16 weeks of age for the Beagle [24]. While our results are in agreement with
the previous observation that 50% of the mature body mass is reached by the age of
14.8 weeks in a larger-bodied breeding line (17 kg, [24]), Salomon and colleagues,
who studied a smaller-bodied line (11.8 kg), reported that their Beagles reached 50%
of the mature body mass with only 7.1 weeks of age [21]. Compared with both
previous studies, the time to reach mature body mass was estimated to be longer in
the current study (95% of the mature mass at 35.1 weeks [21] vs. 38.6 weeks in this
study; 99% after 41.9 weeks [24] vs. 98% after 47.8 weeks). However, a meaningful
comparison among the studies is hindered because the mature body mass
calculated for the dogs in this study probably underestimated their prospective adult
body mass (i.e., calculated mass 17.5 kg vs. parents’ mean 21 kg). Dogs usually
mature physically and gain muscle mass during their first years and thus after
reaching their final body height.
Although sample size in the current study was low and only a limited number of
studies on different breeding lines is available, the comparison of the time lines of the
body mass development of the different sized lines of the Beagle implies 1) that body
mass development varies within a breed and appears to depend on the final body
mass, particularly during the second half of development, and 2) that larger-bodied
lines tend to grow for a longer period. Substantial ontogenetic variation within breeds
was also observed by Weise [18]. On the other hand, some variability in the growth
patterns among breeds of the same body size category was reported by Hawthorne
et al. [24].
In their comprehensive study, Hawthorne et al. [24] reported that 99% of the adult
body mass was reached at about 10 months in toy, small and medium breeds (e.g.,
Papillon: 41 weeks, Cairn Terrier: 43 weeks, Beagle: 42 weeks) and between 11 to
28

Studie I: Ontogenetic allometry of the Beagle
15 months in large and giant breeds (e.g., Labrador Retriever & Great Dane: 52
weeks). In comparison, the Beagles in our study fall between the categories of
medium and large breeds, given their 48 weeks to reach 98% of the mature body
mass.
Body proportions
Heads are relatively large in mammalian juveniles. Therefore, negative allometry
was hypothesized in the current study and it is surprising that the head grew
isometrically in two dogs and showed even positive allometry in one dog. Of the two
heaviest dogs one showed negative allometry and the other showed positive
allometry of the head’s length relative to body mass. The lightest dog’s head grew
isometrically relative to its body mass, resulting in its head being relatively short at 9
weeks but within the normal range at 51 weeks. This is in contrast to Weise [18], who
observed the shortest growth duration in the smallest siblings, resulting in smaller
dogs having shorter heads. In addition to having relatively larger heads, puppies
often appear plumper. As they approach adult size, the dogs become relatively
longer and slimmer. For all dogs in this study, this is reflected by the negative
allometry of the trunk circumference and the positive allometry of the trunk length
compared with body mass and especially by the negative allometry of the head
length vs. trunk length.
Due to the general maturation of the body in cranio-caudal direction (e.g., [39-42]),
greater maturity of the forelimbs compared with the hindlimbs can be expected and
was observed previously [21]. However, the allometric coefficients of the pelvic and
withers height were similar in this study, which is probably related with its relatively
late start at an age of 9 weeks, because higher growth rates were observed for the
hindlimb during early development (e.g., between the 15th and the 29th day, [23]).
Limb proportions
According to Salomon et al. [21], brachium and antebrachium of the Beagle reach
95% of their final length at 230 days and 217 days, respectively. In contrast, the
brachium grew a bit longer in this study (mean: 254 days) and growth duration was
29

Studie I: Ontogenetic allometry of the Beagle
shorter for the antebrachium (173 days). Femur and crus took less time to grow 95%
of their final length in this study (mean: 180 and 206 days, respectively) compared
with the earlier study (233 and 234 days [21]; end of growth according to [23]: 305
and 298 days). This clearly contradicts the observation from the body mass
development, i.e., that larger-bodied lines grow for a longer period. Therefore, the
Beagle line studied herein reached the final segment lengths relatively fast but
gained weight (e.g., by increasing organ and muscles masses) for a longer period
compared to other breeding lines.
Compared with other breeds, the Beagles in the current study also showed 95% of
their final segment lengths earlier than Great Danes (ab: 238.9 days; fe: 262.5 days;
cr: 272.9 days; [43]). The comparison of the growth among different breeds indicated
that larger breeds grow at a higher rate but not necessarily for a longer period
[22,23]. However, Weise [18] pointed out that the times till the dogs are fully grown
may substantially differ among and within breeds as well as among and within litters.
For example, she recorded times to full length from 140 to 243 days for the
antebrachium and from 117 to 243 days for the crus in the poodle [18]. Similarly,
variations of up to 52 days were observed among the siblings of the current study in
reaching 95% of the final segment length. In summary, our results support Weise’s
observations that larger siblings show higher growth rates and that the differences in
the growth curves can be substantial among siblings.
Comparison with other mammals
Based on the ontogenetic allometry of various species, it was observed that
functionally homologous limb segments show more similar growth patterns than
serially homologous segments in mammals [32]. The first finding in the former study
was that the allometric coefficients were more similar between functionally
homologous segments than serially homologous ones. In contrast to previous
observations, the allometric coefficients of the functionally homologous segments
were not comparable in dogs. Rather the growth of the antebrachium resembled that
of the femur and the crus. Femur and crus showed higher allometric coefficients than
scapula and brachium, respectively. This clearly contradicts the expectation of more
30

Studie I: Ontogenetic allometry of the Beagle
similar allometric coefficients between functionally homologous limb segments.
Nevertheless, the typical mammalian intralimb re-proportioning with the proximal
elements showing positive allometry and the very distal ones exhibiting negative
allometry was also observed in the Beagles studied herein (Table 3).
The second observation was that the proximal segments grow more than distal
ones, i.e., limbs show a proximo-distal growth gradient. While this is true for the foreand
hindlimbs of several mammalian species, in the Beagle it can neither be
confirmed for the hindlimb nor for the forelimb (Table 4). Similar to the domestic cat
[2], domestic pig [29], domestic rabbit [35], black-tailed jack rabbit [30], capuchin
monkeys [44,45] as well as other dog breeds [22,38], the antebrachium grew more
than the brachium in the Beagles studied herein. While the antebrachium also grew
more than the scapula in this study, in both previous studies that included the
scapula [29,30], the scapula grew more than any other segment (Table 4).
The third observation concerned the proportions of the segments relative to limb
length [32]. Simulations of three-segmented limb models showed that 1) proportions
close to 1:1:1 are optimal for stability [46,47] and 2) mechanical self-stabilization of
the model is achieved when the length of the middle segment remains constant,
while the lengths of the proximal and distal segments were less critical to the model’s
stability [46]. Accordingly, a greater variability in the proportions of the first and the
third segment was observed across 189 mammalian taxa, while the middle element
was less involved in alterations of the intralimb proportions [25]. In the current study,
the Beagles showed forelimb proportions of 1.2:1.0:1.1 at 9 weeks and 1.1:1.0:1.1 as
adults. Consistent with the model’s prediction, the brachium remained constant in its
proportion of the limb’s anatomical length. In the hindlimb, the segment proportions
were 1.1:1.0:1.1 at 9 weeks and 1.1:1.0:0.9 as adults. In contrast with the model, the
crus increased in its relative length. However, overall, the intralimb proportions were
near the optimum [48] in the juvenile and adult Beagles in this study and comparable
to the segment ratios observed in other breeds of similar body size [49].
In summary, while some principles proposed in a previous study [32] held true for
the Beagles studied herein, others did not. One reason may be that we compared
growth patterns across all mammals for which data were available independent of
31

Studie I: Ontogenetic allometry of the Beagle
their phylogeny, body size, limb posture, habitat or locomotor specialization. Given
that these factors influence the intralimb proportions in mammals [25], they also
probably influence growth patterns. Unfortunately, insufficient data are available at
the moment to be able to assess the impact of these factors on the ontogenetic
allometry of mammals. Furthermore, more studies assembling complete data sets for
all limb segments are necessary to increase our understanding of the growth patterns
in mammals in general and the dog in particular.
2.9. Conclusions
At the age of one year, a Beagle has reached fully grown body height but not body
mass. Up to about 15 weeks of age, Beagles grow particularly intensively, which
should be considered regarding feeding and physical exertion. Compared with its
siblings, a puppy’s size at 9 weeks is a good indication for its adult body size. Among
siblings, growth duration may vary tremendously and seems not to be related to final
body size. Within breeds, we hypothesize a longer duration to physically fully mature
for larger-bodied strains. Throughout ontogeny, the Beagle displayed nearly optimum
intralimb proportions. Neither the forelimbs nor the hindlimbs conformed with the
proximo-distal growth sequence observed previously. Potential factors influencing the
ontogenetic allometry of mammals such as phylogeny, locomotor behavior or body
shape need to be evaluated in future studies.
2.10. List of abbreviations
ab Antebrachium
br Brachium
CI Confidence interval
Cond. Condylus
cr Crus
dors. Dorsalis
Epicond. Epicondylus
fe Femur
hd Head
32

Studie I: Ontogenetic allometry of the Beagle
iso
lat.
LL
ma
maj.
pe
ph
ps
sc
SD
trc
trl
Troch.
Tub.
UL
wi
Isometry
Lateralis
Lower limit of the CI
Manus
Majus
Pelvic length
Pelvic height
Pes
Scapula
Standard deviation
Trunk circumference
Trunk length
Trochanter
Tuberculum
Upper limit of the CI
Withers height
2.11. Competing interests
The authors declare that they have no competing interests.
2.12. Author contributions
DH, PW, IN and NS designed the study and approved the manuscript. DH and NS
collected and analyzed the data and prepared the manuscript.
2.13. Acknowledgements
We wish to thank J. Abdelhadi, S.M. Deban, S. Fischer, V. Galindo-Zamora and K.
Wachs for discussions and help with the analyses, A. Anders, K. Lucas and U. von
Blum for their technical assistance and the animal keepers of the Small Animal Clinic
for their support. This study was supported by the Center of interdisciplinary
prevention of diseases related to professional activities (KIP) founded and funded by
the Friedrich-Schiller-University Jena and the Berufsgenossenschaft Nahrungsmittel
33

Studie I: Ontogenetic allometry of the Beagle
und Gastgewerbe Erfurt and the Hannoversche Gesellschaft zur Förderung der
Kleintiermedizin (HGFK).
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22. Schulze A, Kaiser M, Gille U, Salomon F-V: Vergleichende Untersuchung
zum postnatalen Wachstum der Vordergliedmaße verschiedener Hunderassen.
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leg. Biol Cybern 2001, 84:365-382.
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47. Günther M, Keppler V, Seyfarth A, Blickhan R: Human leg design: optimal
axial alignment under constraints. J Math Biol 2004, 48:623-646.
48. Fischer MS, Witte H: The functional morphology of the three-segmented
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(375):10-17.
49. Fischer MS, Lilje KE: Hunde in Bewegung. Kosmos Verlag 2011:pp. 1-207.
50. Taylor AB: Relative growth, ontogeny, and sexual dimorphism in Gorilla
(Gorilla gorilla gorilla and G. g. beringei): Evolutionary and ecological
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Hum Evol 1994, 26:487-499.
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25:352-361.
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Studie I: Ontogenetic allometry of the Beagle
2.15. Figures
Fig. 1: Recorded measurements. Photograph of dog #4 at the age of 15 weeks to
illustrate the body and segment lengths measured. (The dog’s back was partially
shaved for a joined study.)
39

Studie I: Ontogenetic allometry of the Beagle
Fig. 2: Body mass development of the dogs studied and average growth curve
estimated with the Gompertz function. The parental data were added for comparison.
40

Studie I: Ontogenetic allometry of the Beagle
Fig. 3: Body proportions. Logarithmic plots of withers and pelvic height, trunk and
head lengths as well as trunk circumference vs. body mass. Mean±SD of the
allometric coefficients of the juveniles as well as the information of whether the
respective parameter showed positive (+) or negative (-) allometry are given in the
top left corner of each graph (first line). Numbers in parentheses indicate the UL and
the LL of the 95% confidence intervals (second line). For allometric coefficients of
each dog, see Table l.
41

Studie I: Ontogenetic allometry of the Beagle
Fig. 4: Limb proportions. Logarithmic plots of the segments of the fore- and
hindlimb vs. body mass. Mean±SD of the allometric coefficients of the juveniles as
well as the information of whether the respective parameter showed positive (+) or
negative (-) allometry are given in the top left corner of each graph (first line).
Numbers in parentheses indicate the UL and the LL of the 95% confidence intervals
(second line). For allometric coefficients of each dog, see Table 2.
42

Studie I: Ontogenetic allometry of the Beagle
Fig. 5: Ontogenetic changes of relative segment lengths. Relative segment
lengths were determined as the proportion of the respective segment of the
anatomical limb length (i.e., sum of scapula, brachium, antebrachium and hand as
well as of femur, crus and pes, respectively). The parental data were added in black
for comparison.
43

Studie I: Ontogenetic allometry of the Beagle
2.16. Tables
Tab. 1: Individual parameters of body proportions for all siblings studied. Allometric
coefficient (slope), intercept, standard deviation of the slope (SD slope),
correlation coefficient (R) and the upper and the lower limit of the 95% confidence
interval (95% UL, 95% LL) of all body proportions plotted against body mass on loglog
scales (base 10). Isometry (iso) was given if the slope b=0.333 was within the
confidence interval; otherwise, it was negative (-) or positive (+) allometry. For
comparison, the growth sequence based on the slopes and the respective CIs is
indicated for each dog in the last line. Abbreviations: hd-head length, wi-withers
height, ph-pelvic height, trl-trunk length, trc-trunk circumference.
44

Studie I: Ontogenetic allometry of the Beagle
45

Studie I: Ontogenetic allometry of the Beagle
Tab. 2: Individual parameters of limb segments for all siblings studied. Allometric
coefficient (slope), intercept, standard deviation of the slope (SD slope), correlation
coefficient (R) and the upper and the lower limit of the 95% confidence intervals (95%
UL, 95% LL) of all body proportions plotted against body mass on log-log scales
(base 10). Isometry (iso) was given if the slope b=0.333 was within the confidence
interval; otherwise, it was negative (-) or positive (+) allometry. For comparisons with
previously published results (see Tab. 4), the growth sequences based on the slopes
and the respective CIs are indicated for each dog in the last line. Abbreviations: scscapula,
br-brachium, ab-antebrachium, ma-manus; fe-femur, cr-crus, ps-pes.
46

Studie I: Ontogenetic allometry of the Beagle
47

Studie I: Ontogenetic allometry of the Beagle
Tab. 3: Interspecific comparison of the ontogenetic allometry in various mammalian
species. (+) positive allometry, (-) negative allometry, (iso) isometry. ** Different
measurements among studies (i.e., [30] pelvis, [2] ischium, [50] ilium). Note, two
symbols in ma or ps indicate separate measurements for metacarpus or metatarsus
and phalanges, respectively. Abbreviations: sc-scapula, br-brachium, abantebrachium,
ma-manus; pe-pelvic, fe-femur, cr-crus, ps-pes; m-male, f-female.
Species Forelimb Hindlimb Reference
sc br ab ma pe ** fe cr ps
Domestic cat + + + - + + + - [2]
Black-tailed jack rabbit + + + - + + + - [30]
Western lowland gorilla + + + + [50]
Mountain gorilla
+ m
+ m
[50]
+
- f +
- f
European rabbit + + iso + + iso [35]
Norway rat + iso - + + - [35]
Grey short-tailed
[35]
+ iso - + + iso
opossum
Long-tailed chinchilla iso - - + + - [35]
Tree-shrew
- [32]
+ + - - + iso
iso
Cui
- [32]
+ - - - + -
-
Domestic dog (Beagle) + + + - - + + - this study
** Different measurements among studies (i.e., [30] pelvis, [2] ischium, [50] ilium).
Note, two symbols in ma or ps indicate separate measurements for metacarpus or
metatarsus and phalanges, respectively.
48

Studie I: Ontogenetic allometry of the Beagle
Tab. 4: Interspecific comparison of the growth sequences in various mammalian
species based on the slopes observed in the respective studies. The species in the
upper half of the table show a proximo-distal growth sequence for both fore- and
hindlimbs, while the species in the lower half show deviations from this sequence in
either both or only the forelimb. Note that the separate measurements for metatarsus
and phalanges were combined as pes herein. Abbreviations: sc-scapula, brbrachium,
ab-antebrachium, ma-manus; fe-femur, cr-crus, ps-pes.
Species Forelimb Hindlimb Reference
Grey short-tailed opossum br > ab fe > cr > ps [51,35]
Long-tailed chinchilla br > ab fe > cr > ps [35]
Norway rat br > ab fe > cr > ps [35]
Tree-shrew sc > br > ab fe > cr > ps [32]
Rhesus macaque br > ab fe > cr > ps [52]
Human br > ab fe > cr [53]
Brown-mantled tamarin br > ab fe > cr [54]
African elephant sc > br > ab fe > cr [31]
Asian elephant sc > br > ab fe > cr [31]
Cui sc > br > ab fe > cr > ps [32]
Western lowland gorilla sc > br [50]
Mountain gorilla sc > br [50]
Tuffed capuchin ab > br fe > cr > ps [45]
White-fronted capuchin ab > br fe > cr > ps [45]
Domestic pig sc > ab > br fe > cr [29]
European rabbit ab > br fe = cr > ps [35]
Domestic dog (Beagle) ab > br = sc fe = cr > ps this study
Domestic dog (Great Dane) ab > br fe > cr [38]
Domestic dog (Bernese Mountain dog) ab > br fe > cr [22]
Domestic dog (Rottweiler) ab > br fe > cr [22]
Geoffroy’s spider monkey ab > br cr > fe > ps [44]
White-headed capuchin ab > br cr > fe > ps [44]
Domestic cat ab > br cr > fe > ps [2]
Black-tailed jack rabbit sc > ab > br cr > fe > ps [30]
Virginia opossum la > br ps > fe > cr [51]
49

Studie II: Shift of the CoM in growing dogs
3. Studie II: Shift of the whole-body center of mass in growing dogs
Daniela Helmsmüller 1 , Alexandra Anders 1 , Ingo Nolte 1 and Nadja Schilling 2*
1 Small Animal Clinic, University of Veterinary Medicine Hannover, Foundation,
Bünteweg 9, 30559 Hannover, Germany
2 Institute of Systematic Zoology and Evolutionary Biology, Friedrich-Schiller-
University, Erbertstr. 1, 07743 Jena, Germany
*Correspondence to:
PD Dr. rer. nat. Nadja Schilling; Friedrich-Schiller-Universität; Institut für Spezielle
Zoologie und Evolutionsbiologie; Erbertstr. 1; 07743 Jena; Germany; Phone: ++49
175 5257195; e-mail: nadja.schilling@uni-jena.de
Running headline: Shift of the CoM in growing dogs
Supporting grant information:
This study was supported by the Center of interdisciplinary prevention of diseases
related to professional activities (KIP) founded and funded by the Friedrich-Schiller-
University Jena and the Berufsgenossenschaft Nahrungsmittel und Gastgewerbe
Erfurt and the Hannoversche Gesellschaft zur Förderung der Kleintiermedizin
(HGFK).
This study represents a portion of the Doctoral thesis by DH as partial fulfillment of
the requirements for a Dr. med. vet. degree.
3.1. Abstract
Variation in body shape and thus the antero-posterior distribution of body mass
are associated with differences in the relative position of the center of mass of the
body (CoM). We hypothesized that the ontogenetic changes in body proportions
would affect the location of the whole-body CoM and tested this hypothesis by
examining the vertical ground reaction forces in growing dogs. Six male Beagle
siblings were studied from 9 to 51 weeks of age while they trotted on an instrumented
50

Studie II: Shift of the CoM in growing dogs
treadmill. Ontogenetic shifting of the CoM was evaluated using the vertical force ratio
as well as the stance time ratio of the fore- and hindlimbs. The ratio of the thorax and
abdomen diameters was determined to assess the developmental changes in trunk
shape. As in adult dogs, the forelimbs carried a greater proportion of the body weight
than the hindlimbs at all ages. When the dogs were younger, peak vertical force
occurred earlier during stance in the hindlimbs but not the forelimbs. Both the
increasing ratio of the vertical force (i.e., peak force, impulse) and the increasing ratio
of the stance times indicate a net cranial shift of the CoM during growth. Associated
with that, the forelimbs supported an increasing (59% vs. 63%) and the hindlimbs
bore a decreasing proportion (41% vs. 37%) of the body weight during ontogeny. The
observed net cranial shift of the CoM is likely the consequence of the substantial
change in trunk shape and thus of the growth patterns of the inner organs.
Key words: kinetic, Canis, development, gait analysis
3.2. Abbreviations
Ab abdomen
BW body weight
CoM center of body mass
FL forelimb
GRF ground reaction forces
HL hindlimb
IFz vertical impulse
MFz mean vertical force
PFz peak vertical force
PW postnatal week
SI symmetry index
Th thorax
U Froude number
51

Studie II: Shift of the CoM in growing dogs
3.3. Introduction
Natural variation in body shape and the antero-posterior distribution of body mass
are associated with differences in fore- vs. hindlimb loading and the relative position
of the center of mass of the body (CoM). While in quadrupeds with heavy tails (e.g.,
alligators) or relatively large hindlimb muscles (e.g., many primates) the CoM is more
caudal and the forelimbs support less than half of the body weight, the CoM is
located relatively cranial in most quadrupedal mammals and the forelimbs carry more
than half of the body’s weight (e.g., Rollinson and Martin, 1981; Pandy et al., 1988;
Kimura, 1992; Rumph et al., 1994; Demes et al., 1994; Lee et al., 1999; Walter and
Carrier, 2002; Aerts et al., 2003; Willey et al., 2004; Schmidt, 2005; Hanna et al.,
2006).
Among the quadrupeds with a cranial location of the CoM, species with massive
forelimbs and/or heavy heads bear a comparatively greater proportion of their body
weight on the forelimbs compared with species with rather muscular hindlimbs (e.g.,
Rollinson and Martin, 1981; Demes et al., 1994). For example, the fore- to hindlimb
proportion is 52% to 48% in the cheetah and 66% to 34% in the camel (Rollinson and
Martin, 1981). Among closely related species, variation in muscle mass distribution
due to for example differences in locomotor adaptation or male agonistic behavior
have also been described (Grand, 1997). Additionally to these interspecific
variations, differences in limb loading were observed among breeds with different
builds. For example, warmbloods load their forelimbs more than quarter-horses
(Back et al., 2007). Dogs bred for high acceleration and speed (i.e., with large
hindlimb muscles; Williams et al., 2008) support a relatively greater proportion of their
body weight with the hindlimbs than dogs that have a more muscular chest and
larger heads (Bertram et al., 2000; Voss et al., 2011). Thus, the Rottweiler bears
64% of its body weight on the forelimbs compared with 57% in the Borzoi (Voss et
al., 2011).
Physiological variation in an individual’s antero-posterior body mass distribution
occurs during ontogeny due to the allometric growth of muscles, bones and organs.
Mammalian juveniles, for example, have relatively large heads compared to adults
(e.g., Trotter et al., 1975; Kimura, 1987; Schilling and Petrovitch, 2006; Helmsmüller
52

Studie II: Shift of the CoM in growing dogs
et al., subm.). This together with the hindlimbs increasing in length and/or muscularity
more than the forelimbs leads to a net caudal translation of the CoM and thus a
decreasing relative forelimb loading in various growing mammals (rhesus macaque:
Grand, 1977; Turnquist and Wells, 1994; chimpanzee: Kimura, 1987; Japanese
macaque: Kimura, 2000; koala: Grand and Barboza, 2001; yellow baboon: Shapiro
and Raichlen, 2006; squirrel monkey: Young, 2012). On the other hand, mammalian
juveniles often appear plump and lack the athletic body shape that their adult
conspecifics show. Developing the adult appearance could therefore be associated
with a net cranial translation of the CoM in species like the dog that undergo a more
pronounced change in trunk shape. Furthermore, in contrast to the hindlimbdominated
species that have been studied previously, dogs provide a test for the
ontogenetic shifting of the CoM in a species that supports a greater proportion of the
body weight with the forelimbs.
In order to test whether mammals with a cranial location of the CoM also show a
net caudal translation of their CoM or whether they experience a net cranial shift
during growth, we studied the ontogenetic changes in the fore- vs. the hindlimb
loading in dogs. Because the distribution of body mass is reflected by the fore- to
hindlimb relationship of the vertical force (e.g., Rollinson and Martin, 1981; Budsberg
et al., 1987; Lee et al., 2004; Voss et al., 2011), we recorded the ground reaction
forces (GRF) in the dogs while trotting at steady speed on an instrumented treadmill.
Three parameters of the force distribution between the fore- and the hindlimbs were
tested: peak and mean vertical force as well as vertical impulse. Additionally to
evaluating the fore- to hindlimb vertical force ratio, we determined the stance
durations of the limbs, because a higher fraction of the vertical impulse of a limb is
associated with a relatively higher duty factor and the ratio between fore- and
hindlimb stance times has been suggested to reflect the antero-posterior mass
distribution of trotting quadrupeds (Lee et al., 2004; Witte et al., 2004). To evaluate
the change in trunk shape during postnatal development, we determined the ratio
between the diameters of the thorax and the abdomen in the growing dogs.
----- Figure 1 ------
53

Studie II: Shift of the CoM in growing dogs
3.4. Animals and Methods
Dogs
Six male Beagle siblings (Canis lupus familiaris, Linnaeus 1758) from the same
litter were used in this longitudinal study. The dogs were from a breeding colony of
the University of Veterinary Medicine Hannover (Germany) and came to the Small
Animal Clinic at the age of 9 weeks (i.e., PW9). During the study period, all dogs
underwent two standard orthopedic exams, one at PW14 and one at PW50, which
confirmed that the dogs were sound. For the gait analysis, the puppies were gently
introduced to ambulating on the treadmill when they were 9 weeks old. All
experiments were carried out in accordance with the German Animal Welfare
guidelines and notice was given to the Ethics committee of Lower Saxony
(Germany).
Data collection
GRF measurements started at PW9 and continued until PW51. Data were
collected weekly up to PW20, fortnightly up to PW32 and monthly henceforth.
Additionally to the GRF recordings, various morphometric measurements (e.g.,
segment and limb lengths) were taken for a related study (Helmsmüller et al., subm.)
and the dogs were photographed in lateral perspective standing as balanced and
square as possible (Fig. 1). From all recordings, data from PW11, 13, 19, 22, 26, 30,
43 and 51 were selected for further analysis. Two dogs could not participate in the
data collection at PW19 and were therefore measured the following week (i.e.,
PW20).
During GRF data collection, the dogs trotted on a horizontal treadmill with four
separate belts and integrated force plates underneath each belt (Model 4060-08,
Bertec Corporation, Columbus, OH, USA). Because of their small body size, the
puppies trotted on one side of the treadmill allowing the forces exerted by the foreand
the hindlimbs to be recorded separately (sample rate 1,000 Hz). Separate force
curves for the left and the right limbs were nevertheless obtained because the duty
factor was less than 0.5 during all recordings. To identify whether the right or the left
54

Studie II: Shift of the CoM in growing dogs
limbs were exerting force, a digital camera synchronized with the GRF recordings
imaged the dogs from the lateral perspective (NVGS60, Panasonic).
Kinetic data were collected and analyzed using Vicon Nexus (Vicon Motion
Systems Ltd., Oxford, UK). During each session, at least 3 trials per dog were
obtained lasting about 30 seconds and covering approximately 65 strides. Of these,
10 valid steps (i.e., without overstepping) were analyzed per dog and age. The
selected strides were not always consecutive because the dogs, particularly when
very young, did not run as consistently as when they were older. Touch down and lift
off events were determined manually using the vertical force curves; force threshold
was set at 5% of the dog’s body weight. Then, the force data were time-normalized to
100% stance duration (i.e., 101 data points) using linear interpolation and exported to
Microsoft Excel together with the temporal gait parameters (i.e., stance duration in s).
Data analysis
Vertical force data from the 10 steps were averaged per dog and normalized to the
dog’s body weight (BW) using equation (1):
(1) GRFs (%BW) = vertical force*100/(body mass*9.81 m/s2)
The vertical GRF parameters compared among the ages were peak and mean
vertical force as well as vertical impulse. Additionally, symmetry indices for the foreand
hindlimbs, time to peak vertical force (in % stance duration) and the distribution
of the dog’s body weight among the four limbs were determined. Body weight
distribution was calculated using equation (2):
(2) % BW bearing = vertical force of the limb/total vertical force of all limbs*100
Symmetry indices (SI) were determined using equation (3) (according to Herzog et
al., 1989):
(3) SI = 100 * (Xl - Xr)/(0.5* (Xl + Xr))
with X being the vertical force of the left (l) and right (r) fore- or hindlimb averaged
across the ten steps. Furthermore, the ratio of the stance times of the fore- and
hindlimbs (i.e., forelimb stance time divided by hindlimb stance time) were
determined.
55

Studie II: Shift of the CoM in growing dogs
Treadmill speed had to be matched more or less to the preferred speed of the
dogs (i.e., the speed at which they trotted most comfortably) in order to record as
many valid strides as possible. Because absolute speed cannot be compared among
different-sized individuals, Froude number (U) was calculated using the equation (4):
(4) U = v2/g*l
v represents absolute speed (in m/s), g is gravitational acceleration (9.81 ms-2)
and l is hindlimb length (based on Alexander and Jayes, 1983).
To evaluate the change in trunk shape, the diameters of the thorax and the
abdomen were measured in the photographs using Adobe PhotoShop Version 5. The
thoracic diameter was determined posterior to the forelimb at the deepest point of the
sternum; the abdominal diameter was measured cranial to the prepuce (Fig. 1).
Then, the ratio of the two lengths was calculated. A ratio of 1.0 indicates a
rectangular area in the image (i.e., a cylindrical trunk shape), while a ratio >1.0
indicates a trapezoid (i.e., a conical trunk shape with the abdominal diameter being
smaller than the thoracic one).
Statistics
The data were tested for normal distribution using the Kolmogorov-Smirnov-Test.
Differences among the vertical force or the stance duration ratios as well as the
thorax-to-abdomen ratio and the ages were tested using a one-way analysis of
variance (ANOVA) for repeated measures followed by post hoc Tukey test. P values
of p

Studie II: Shift of the CoM in growing dogs
puppies’ force parameters were as symmetrical as those of adult dogs despite the
puppies’ seemingly more irregular gait.
----- Table 1 -----
During the course of the study, the dogs’ preferred trotting speeds increased and
therefore the Froude number differed slightly but significantly between the first and
the last recordings (PW11: U=0.5±0.1, PW51: U=0.9±0.1; Tab. 2). Consequently,
younger dogs trotted at treadmill speeds at which they still walked when older.
Because both vertical force and temporal gait parameters are dependent on speed
(see discussion), we will focus on fore- to hindlimb ratios of these parameters in the
following. Fore- and hindlimb values are detailed in the supplementary file (Tab. S1).
----- Table 2 -----
At all ages, peak vertical force and vertical impulse were significantly greater in the
forelimbs than the hindlimbs, indicating that the CoM was in a relatively cranial
position at all ages (Fig. 2, Tab. 3). The ANOVA revealed that both peak vertical
force and vertical impulse showed significant differences among the ages; with age,
they increased in the forelimb and consequently decreased in the hindlimb.
Accordingly, the fraction of the body weight supported by the forelimbs increased
from 59.2 1.7% to 62.9 1.9% (PFz) while that of the hindlimbs decreased from
40.8 1.7% to 37.1 1.9% during the course of the study. Similarly, vertical impulse
shifted by ca. 4% of the body weight from caudal to cranial. In contrast, mean
normalized vertical force was not significantly different among sessions (Tab. 3). The
ratio between fore- and hindlimb stance times increased significantly; thus, stance
time of the forelimb increased relative to the stance time of the hindlimb (Tab. 2).
While the time to peak vertical force did not change with age in the forelimbs, it
increased significantly in the hindlimb indicating that maximum force occurred earlier
during stance phase when the dogs were younger (Tab. 4).
The ratio of the thoracic vs. the abdominal diameter indicated that the trunk shape
of the puppies was nearly cylindrical (i.e., thorax-to-abdomen ratio 1.1 at PW11; Tab.
4). During the study period, the thorax-to-abdomen ratio increased significantly, so
that the trunk shape resembled a frustum at the end of the study (i.e., thorax-toabdomen
ratio 1.3 at PW51; Tab. 4).
57

Studie II: Shift of the CoM in growing dogs
----- Tables 3 and 4 -----
3.6. Discussion
Influence of speed on force and stance parameters
In the current study, Froude number significantly increased between 11 and 51
weeks of age. Because many gait parameters depend on locomotor speed, the
observed changes in the vertical force and the stance time ratios may potentially
result from differences in speed rather than age. In adult dogs, for example, peak
vertical force increases and vertical impulse decreases with increasing trotting
velocity (Riggs et al., 1993; McLaughlin and Roush, 1994, Voss et al., 2010).
Because maximum vertical force increases more in the forelimbs than the hindlimbs
when dogs trot faster, the increase in the fore- to hindlimb peak vertical force ratio
observed in the current study may partially be explained by the increase in relative
velocity with age. However, compared with the change in the peak vertical force ratio
observed in this study (ca. 4%), the speed related changes reported for adult dogs
across a similar change of relative velocity were small (ca. 2%; Riggs et al., 1993;
McLaughlin and Roush, 1994). Furthermore, in adult trotting dogs, the vertical
impulse of fore- and hindlimbs decreases at similar rates with increasing speed and
therefore impulse ratio is independent of speed (Riggs et al., 1993; McLaughlin and
Roush, 1994; see also Witte et al., 2004). In contrast, the fore- to hindlimb impulse
ratio increased significantly with age in the current study; that is, the forelimbs’
vertical impulse was relatively larger in older dogs than puppies. This observation
resembles results from adult dogs, in which experimental loading of the pectoral
girdle resulted in an increase of the vertical impulse ratio (Lee et al., 2004). In
summary, our data suggest that the position of the whole-body CoM undergoes a
net-cranial translation in growing dogs and accordingly the forelimbs support a
relatively smaller proportion of the body weight in puppies than adult dogs.
Similar to other mammals, when dogs increase locomotor speed, stance time
decreases (Arshavskii et al., 1965; McLaughlin and Roush, 1994; Maes et al., 2008).
Because stance duration decreases more in the forelimbs than the hindlimbs, stance
time ratio decreases when adult dogs trot faster (McLaughlin and Roush, 1994). In
58

Studie II: Shift of the CoM in growing dogs
contrast, the stance time ratio between fore- and hindlimbs increased during the
course of this study despite an increase in relative velocity. Relative fore- and
hindlimb duty factors have been suggested to reflect the antero-posterior mass
distribution of trotting quadrupeds and adding mass to the forelimb led to an increase
in the fore- to hindlimb stance time ratio (Lee et al., 2004). Therefore, the increase in
the stance time ratio observed herein corroborates our conclusion that the CoM shifts
cranially when dogs grow.
Ontogenetic changes in limb loading and the position of the CoM
Between PW11 and PW13 (three dogs) or PW19 (three dogs), the time to peak
vertical force increased significantly in the hind- but not the forelimbs. Therefore,
loading rate was greater in the hindlimbs when the dogs were very young. Various
factors influence the shape of the GRF curve such as the geometric compression of
the leg spring due to the forward motion of the body as well as the limb’s angle of
attack, stiffness and anatomical design (Farley et al., 1993; Witte et al., 2004).
Spring-mass-model simulations, for example, have shown that the trajectory of the
CoM during a stride depends, among other factors, on the angle of attack (Farley et
al., 1993; Seyfarth et al., 2002). That is, steeper angles are associated with a
relatively earlier minimum in the trajectory of the CoM and accordingly an earlier
peak of the vertical force. Compared with when older, puppies appear to protract
their limbs less and hit the ground in a more vertical paw trajectory and a more
flatfooted manner; thus, they seem to have a lower angle of limb retraction before
touch down and therefore a greater rate of limb compression. One consequence of a
steeper angle of touch down is that limb muscle force must be build up more rapidly
(Seyfarth et al., 2002). However, without the according kinematic and electromyographic
data, it remains open whether the increased loading rate in the hindlimbs of
puppies is the consequence of differences in limb behavior.
Numerous studies have shown that the whole-body CoM is situated relatively
cranial in dogs (Bryant et al., 1987; Budsberg et al., 1987; Rumph et al., 1994;
DeCamp, 1997; Lee et al., 1999; ; Bertram et al., 2000; McLaughlin, 2001; Fanchon
et al., 2006; Bockstahler et al., 2007; Walter and Carrier, 2007; Katic et al., 2009;
59

Studie II: Shift of the CoM in growing dogs
Mölsa et al., 2010; Kim et al., 2011; Voss et al., 2011) and, as this and one previous
study examining dogs between PW4 and PW15 show (Biknevicius et al., 1997), this
is true from early on in life. Therefore, in puppies and adult dogs, the forelimbs
consistently support a greater proportion of the body weight than the hindlimbs. At
the end of this study, at PW51, load distribution of the dogs studied herein was
comparable with adult individuals of the same breed (Abdelhadi et al., 2013).
Variation in how much the fore- vs. the hindlimbs support in adult dogs, however,
is related to morphological differences among breeds (i.e., the antero-posterior
distribution of body mass). Sighthounds such as Greyhounds or Borzoi show lower
vertical force ratios compared to other breeds such as Labrador Retriever,
Rhodesian Ridgeback or Rottweiler (Bertram et al., 2000; Mölsa et al., 2010; Kim et
al., 2011; Voss et al., 2011). Thus, depending on morphology, the specific position of
the whole-body CoM varies in adult dogs. Similarly, morphological variation due to
growth results in changes in the weight-supporting characteristics of fore- vs.
hindlimbs in mammals (Grand, 1977; Turnquist and Wells, 1994; Kimura, 1987;
Kimura, 2000; Grand and Barboza, 2001; Shapiro and Raichlen, 2006; Young, 2012;
this study). Both, vertical force and stance time ratios evaluated in the current study
indicate a net cranial shift of the CoM in growing dogs. This is in contrast to the
previous studies, which consistently reported a net caudal shift of the CoM and thus
a relative decrease in forelimb and conversely an increase in hindlimb loading with
age (Grand, 1977; Turnquist and Wells, 1994; Kimura, 1987; Kimura, 2000; Grand
and Barboza, 2001; Shapiro and Raichlen, 2006; Young, 2012).
At least two observations may explain the net cranial translation of the CoM in
growing dogs. First, the postural index (i.e., withers or pelvic height divided by the
sum of the segment lengths) decreases more in the hindlimbs than the forelimbs
(from 1.17 to 1.07 and 1.31 to 1.24 between PW11 and PW51, respectively; D.
Helmsmüller, unpubl. data). Therefore, similar to growing horses (Grossi and Canals,
2010), older dogs have relatively more erect hindlimbs than when they are younger.
The increasingly erect hindlimbs result in a postural change of the body that is
consistent with a net cranial translation of the CoM.
60

Studie II: Shift of the CoM in growing dogs
Second, puppies have a relatively voluminous belly and a cylindrical rather than
the conical body form that adults show (Fig. 1). Abdominal organs such as spleen or
kidneys show negative allometry, while the heart (Lützen et al., 1976; but see
Deavers et al., 1972) and the stomach exhibit positive allometry in various mammals
(guinea pig: Bessesen and Carlson, 1923; dog: Deavers et al., 1972; Lützen et al.,
1976; rat: Stewart and German, 1999). Furthermore, to fuel ontogenetic growth and
provide the developing body with the tissue necessary for digestion and absorption of
high dietary loads, the small intestine is enlarged in growing animals. For example,
Beagle puppies at PW9 have a small intestine that is 33% longer, weighs 45% more,
has 40% more mucosa and 35% more surface area compared with adults (Paulsen
et al., 2003). Taken together, the growth patterns of the inner organs and particularly
of the small intestine are in accordance with a cranial shift of the CoM. On the
contrary, muscularity increases more in the hindlimbs than the forelimbs in cursorial
mammals such as bovids (Grand, 1991), and dogs, as other mammals, show
negative allometry of their heads (Helmsmüller et al., subm.). Nevertheless, although
the latter two observations would be consistent with net caudal shift of the CoM, our
results indicate that the growth patterns of the inner organs dominate the limb loading
changes in growing dogs.
3.7. Acknowledgments
We thank our colleagues J. Abdelhadi, S. Fischer, V. Galindo-Zamora and P.
Wefstaedt for discussions, K. Lucas for technical assistance and the animal keepers
of the Small Animal Clinic for their support.
3.8. Conflict of interest statement
None of the authors has any financial or personal relationship that could inappropriately
influence or bias the content of the paper.
61

Studie II: Shift of the CoM in growing dogs
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3.10. Figures
Fig. 1: One of the subjects at four different time points during development. Size
was scaled to the same trunk length to illustrate the changes in body proportions and
particularly in trunk shape. The vertical lines indicate where the thoracic and
abdominal diameters were measured to evaluate the change in trunk shape during
the study period. (The two sites shaved on the back provided data for a separate
study.)
67

Studie II: Shift of the CoM in growing dogs
Fig. 2: Vertical force curves of the fore- and the hindlimbs time-normalized to the
stance duration of the forelimbs. Plotted are the means from the six dogs, error bars
indicate standard deviation. Note, the decrease of the hindlimb’s stance time relative
to that of the forelimbs and the increasing force difference between fore- and
hindlimbs. *Two dogs were studied at PW20.
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Studie II: Shift of the CoM in growing dogs
3.11. Tables
Table 1: Symmetry indices (mean ± s.d.) of the vertical force parameters for all
dogs at the different ages. Perfect symmetry is given at SI=0. Physiological ranges
are up to 4% and 6% difference for the fore- and the hindlimbs, respectively
(Budsberg et al., 1993). Negative values indicate that the parameters were greater
for the right than the left limb; positive values indicate the reverse.
PW PFz MFz IFz
FL HL FL HL FL HL
11 -0.2 ± 1.5 -0.2 ± 1.3 -0.3 ± 3.6 3.6 ± 3.0 -0.2 ± 4.1 4.4 ± 4.5
13 -0.9 ± 1.7 1.7 ± 2.5 0.0 ± 2.0 1.1 ± 2.5 0.8 ± 4.3 0.9 ± 3.6
19* -0.2 ± 0.4 0.0 ± 1.3 -1.9 ± 3.1 -0.1 ± 2.4 -1.9 ± 1.4 -0.2 ± 3.7
22 -0.3 ± 1.3 0.3 ± 1.7 -1.5 ± 2.7 0.8 ± 3.0 -0.1 ± 4.4 1.6 ± 5.7
26 -0.4 ± 1.6 -0.1 ± 1.6 -0.3 ± 2.5 -0.7 ± 3.6 -0.3 ± 3.3 -2.5 ± 5.6
30 0.2 ± 0.9 -0.4 ± 2.0 -0.1 ± 2.4 0.6 ± 2.4 0.7 ± 3.9 1.5 ± 4.3
43 -0.1 ± 1.8 -1.0 ± 1.9 1.1 ± 3.1 0.2 ± 2.5 0.3 ± 3.6 1.2 ± 3.3
51 0.3 ± 2.7 -0.5 ± 1.6 0.6 ± 2.6 0.1 ± 4.2 -0.2 ± 1.9 1.0 ± 7.1
*Note that two individuals were measured at PW20.
Abbreviations: PFz, peak vertical force; MFz, mean vertical force; IFz, vertical
impulse; FL, forelimb; HL, hindlimb; PW, postnatal week.
Table 2: Stance duration (mean ± s.d. in s) for the fore- and hindlimbs and stance
duration ratio as well as Froude number (mean ± s.d.) for all dogs at the different
ages.
PW FL HL FL/HL U
11 0.20 ± 0.01 0.19 ± 0.01 1.05 ± 0.06 a 0.53 ± 0.09 a
13 0.22 ± 0.01 0.20 ± 0.01 1.07 ± 0.02 b 0.52 ± 0.09 b
19* 0.23 ± 0.01 0.22 ± 0.01 1.06 ± 0.02 c 0.56 ± 0.04 c
22 0.23 ± 0.01 0.21 ± 0.01 1.09 ± 0.05 d 0.62 ± 0.04 d
26 0.22 ± 0.00 0.19 ± 0.01 1.15 ± 0.05 a,b,c 0.78 ± 0.05 a,b,c,d,e
30 0.22 ± 0.01 0.19 ± 0.01 1.16 ± 0.05 a,b,c 0.85 ± 0.06 a,b,c,d
43 0.22 ± 0.00 0.18 ± 0.01 1.18 ± 0.05 a,b,c,d 0.87 ± 0.08 a,b,c,d
51 0.21 ± 0.01 0.18 ± 0.02 1.15 ± 0.08 a,b,c 0.93 ± 0.11 a,b,c,d,e
*Note that two individuals were measured at PW20.
Abbreviations: FL, forelimb; HL, hindlimb; PW, postnatal week, U Froude number.
Paired letters in subscript refer to a significant difference (p

Studie II: Shift of the CoM in growing dogs
Table 3: Mean load distribution (mean ± s.d. in %BW) between the fore- and the
hindlimbs of all dogs at the different ages.
PW PFz MFz IFz
FL HL FL HL FL HL
11 59.2 ± 1.7 a 40.8 ± 1.7 a 61.7 ± 5.0 38.3 ± 5.0 62.4 ± 4.7 a 37.6 ± 4.7 a
13 60.6 ± 1.8 b 39.4 ± 1.8 b 61.6 ± 0.8 38.4 ± 0.8 63.0 ± 1.0 b 37.0 ± 1.0 b
19 61.8 ± 2.2 38.2 ± 2.2 61.1 ± 1.8 38.9 ± 1.8 62.5 ± 1.2 c 37.5 ± 1.2 c
*
22 61.7 ± 1.9 38.3 ± 1.9 61.3 ± 1.8 38.7 ± 1.8 63.3 ± 1.2 d 36.7 ± 1.2 d
26 62.8 ± 2.4 a 37.2 ± 2.4 a 62.6 ± 2.1 37.4 ± 2.1 65.8 ± 1.4 34.2 ± 1.4
30 63.1 ± 2.9 a,b 36.9 ± 2.9 a 62.5 ± 2.7 37.5 ± 2.7 66.0 ± 1.6 34.0 ± 1.6
43 63.7 ± 2.1 a,b 36.3 ± 2.1 a,b 63.6 ± 1.6 36.4 ± 1.6 67.4 ± 0.8 a,b,c,d 32.6 ±
0.8 a,b,c,d
51 62.9 ± 1.9 a 37.1 ± 1.9 a 63.3 ± 2.0 36.7 ± 2.0 66.5 ± 0.7 a,c 33.6 ± 0.7 a,c
*Note that two individuals were measured at PW20.
For abbreviations, see Table 1. For explanation of the subscripts, see Table 2.
Table 4: Time to peak force (mean ± s.d. in % of stance duration) of the fore- and
hindlimbs and thorax-to-abdomen ratio (mean ± s.d.) for all dogs at the different
ages.
PW FL HL Th/Ab
11 47.7 ± 4.1 39.8 ± 3.3 a 1.09 ± 0.06 a
13 44.8 ± 4.8 41.8 ± 2.6 b 1.07 ± 0.04 b
19* 42.4 ± 2.2 44.6 ± 2.9 a 1.13 ± 0.05 c
22 44.5 ± 2.4 45.6 ± 2.5 a 1.21 ± 0.05 a,b,d
26 45.3 ± 2.2 46.7 ± 2.8 a,b 1.21 ± 0.06 a,b,e
30 45.5 ± 2.1 45.3 ± 1.1 a 1.28 ± 0.06 a,b,c
43 44.7 ± 1.7 46.5 ± 2.1 a,b 1.31 ± 0.05 a,b,c,d,e
51 46.4 ± 1.3 46.2 ± 0.9 a,b 1.27 ± 0.05 a,b,c
*Note that two individuals were measured at PW20.
For abbreviations, see Table 1; Th, thorax; Ab, abdomen. For explanation of the
subscripts, see Table 2.
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Studie II: Shift of the CoM in growing dogs
Supplementary data
Tab. S1: Vertical force parameters (mean ± s.d. in %BW) for all dogs at the
different ages.
PW PFz MFz IFz
FL HL FL HL FL HL
11 101.0 ± 7.0 69.9 ± 7.1 59.7 ± 7.6 36.8 ± 3.5 12.1 ± 1.8 7.2 ± 0.5
13 107.1 ± 6.4 69.7 ± 4.3 59.6 ± 3.2 37.2 ± 2.2 12.8 ± 0.8 7.5 ± 0.7
19* 114.1 ± 3.1 70.7 ± 5.7 60.8 ± 1.6 38.8 ± 2.7 13.9 ± 0.8 8.3 ± 0.5
22 118.0 ± 6.4 73.2 ± 4.6 62.1 ± 2.6 39.2 ± 2.1 14.4 ± 0.7 8.3 ± 0.5
26 124.1 ± 5.8 73.7 ± 5.7 64.6 ± 2.9 38.6 ± 2.1 14.1 ± 0.5 7.3 ± 0.4
30 127.4 ± 4.7 75.0 ± 9.0 65.3 ± 2.1 39.2 ± 3.9 14.1 ± 0.4 7.3 ± 0.5
43 125.9 ± 3.4 71.9 ± 5.6 65.7 ± 1.6 37.6 ± 1.9 14.2 ± 0.7 6.9 ± 0.3
51 124.4 ± 5.3 73.3 ± 4.8 64.6 ± 1.6 37.5 ± 2.7 13.5 ± 0.5 6.8 ± 0.3
*Note that two individuals were measured at PW20.
Abbreviations: PFz, peak vertical force; MFz, mean vertical force; IFz, vertical
impulse; FL, forelimb; HL, hindlimb; PW, postnatal week.
71

Diskussion
4. Diskussion
In dieser Studie wurden die Proportionsänderungen während des Wachstums
beim Beagle und ihr Einfluss auf die kraniokaudale Lage des Körpermasseschwerpunktes
während der Ontogenese untersucht. Erstmalig wurde dabei die Skapula als
lokomotorisch relevantes Element der Vorderextremität in die morphometrische
Analyse der Ontogenese des Hundes einbezogen. Dieses proximale Segment der
Vordergliedmaße trägt wie bei anderen Säugetieren maßgeblich zum Rumpfvortrieb
bei (FISCHER u. LILJE 2011). Ihr Drehpunkt liegt in den symmetrischen Gangarten
wie Schritt und Trab auf der gleichen Höhe wie der des Femurs, und beide
proximalen Elemente ähneln sich in ihrer Bewegungstrajektorie und ihrem
Bewegungsumfang. Damit entsprechen sich bei den Säugetieren nicht seriell
homologe Segmentabschnitte funktionell, während bei Vertretern der Lissamphibia
oder der Lepidosauria die ursprünglich seriellen Gliedmaßenabschnitte auch
funktionell homolog sind (BARCLAY 1946, JENKINS & GOSLOW 1983). Der
Einschluss der Skapula in die vorliegende Untersuchung ermöglichte eine
vergleichende Betrachtung der ontogenetischen Entwicklung der sich funktionell
entsprechenden Vorder- und Hintergliedmaßenabschnitte. Im Unterschied zu
früheren Befunden an nicht-cursorialen Säugetieren (SCHILLING u. PETROVITCH
2006), unterschieden sich die Entwicklungsverläufe der funktionell homologen
Abschnitte beim Beagle, indem Femur und auch Crus höhere positive Allometrie
zeigten als Skapula und Brachium (Fe: 0,44 Cr: 0,43 vs. Sk: 0,40 Br: 0,41).
Simulationen mit variierenden relativen Längen eines dreisegmentigen Feder-
Masse-Modells zeigten, dass das Modell hohe selbststabilisierende Eigenschaften
hatte, wenn sich die Abschnitte in ihrer Länge wie 1:1:1 verhielten (SEYFARTH
2001, GÜNTHER 2004). Insbesondere die Länge des mittleren Abschnittes
(Brachium und Crus) hatte einen entscheidenden Einfluss darauf, ob das Modell
nach Perturbation zu seiner stabilen Bewegungstrajektorie zurückkehrte oder nicht.
Im Unterschied dazu spielten die Längen des proximalen und des distalen
Abschnittes eine untergeordnete Rolle. Die Ergebnisse der vorliegenden Arbeit
zeigten, dass bei Beaglen sehr früh in der Ontogenese ein nahezu optimales
Längenverhältnis der Extremitätenabschnitte vorliegt (Vordergliedmaßen 1,2:1,2:1,1
72

Diskussion
PW9, 1,1:1,0:1,1 PW51; Hintergliedmaßen 1,1:1,0:1,1 PW9, 1,1:1,0:0,9 PW51). Im
Unterschied zu Befunden an anderen Säugetieren (SCHMIDT u. FISCHER 2009)
blieb in Übereinstimmung mit den Modellvorhersagen nur die relative Länge des
Brachiums an der Gesamtlänge des Vorderbeines konstant in der Ontogenese,
während die relative Länge des Crus an der Gesamtlänge des Hinterbeines zunahm.
Weitere Verschiebungen der Segmentproportionen innerhalb der Extremitäten
betrafen die relative Längenzunahme des Antebrachiums und Femur und die relative
Längenabnahme der Autopodien (Manus und Pes), die in Übereinstimmung mit
früheren Befunden an verschiedenen Säugetieren sind und die typischen Proportionsverschiebungen
bei Säugetieren für die Hinterextremitäten bei Hunden
bestätigen.
Die beobachteten Proportionsverschiebungen innerhalb der Extremitäten haben
biomechanische Konsequenzen; beispielsweise ändern sich dadurch die Hebelarmverhältnisse
der Muskulatur. Dies ist möglicherweise ein Grund dafür, dass es
während des Wachstums zu orthopädischen Problemen kommen kann. Zur
Beurteilung der physiologischen Proportionsverschiebungen können die in der
vorliegenden Arbeit erhobenen Daten als Referenz zumindest für die Rasse Beagle
dienen. Inwiefern die beobachteten morphometrischen Veränderungen für andere
Rassen gelten, die beispielsweise als Adulti deutlich von der Norm abweichende
Extremitätenproportionen zeigen, wie z.B. der Dackel oder der Scottish Terrier
(FISCHER u. LILJE 2011), bleibt zu prüfen. Darüber hinaus sollten zukünftige
Studien die Skapula in ihre Erhebungen einbeziehen, um so eine zunehmend
vollständigere Befundlage zu schaffen.
Weitere morphometrische Veränderungen in der Ontogenese betrafen die relative
Länge des Kopfes und die Proportionen des Rumpfes. Wie alle Säugetiere haben
auch junge Hunde einen relativ großen Kopf; so dass die Ergebnisse der vorliegenden
Arbeit im Mittel ein negativ allometrisches Wachstum für die Kopflänge zeigten.
Dadurch besitzt der erwachsene Hund einen relativ kürzeren Kopf bezogen auf die
Körpermasse oder -länge als der junge Hund. Die erhobenen Rumpfproportionen
zeigten ein negatives allometrisches Wachstum des Umfanges und eine relative
Zunahme der Rumpflänge. Zusätzlich nahm das Verhältnis Thorax zu Abdomen
73

Diskussion
während des Messzeitraums zu (1,1 bis 1,3; Tab. 4, Studie 2), sodass sich die
Rumpfform von einer eher zylindrischen Form beim Welpen zu einer deutlich
taillierten und konischen Form beim adulten Hund änderte.
Während die relative Abnahme der Kopfgröße gemeinsam mit der stärker
zunehmenden Muskularisierung der Hinterextremität (GRAND 1991) für eine
Verschiebung des CoM nach kaudal sprechen würde, lässt sich aus der Veränderung
der Rumpfform eine kraniale Verschiebung vermuten. Die kinetischen und
metrischen Analysen zeigten eine kraniale Verschiebung des Körpermasseschwerpunktes
um im Mittel ca. 4%, im Unterschied zu allen vorangegangenen Studien an
Primaten, die eine kaudale Verschiebung berichteten (KIMURA 1987, 2000;
TURNQUIST u. WELLS 1994; YOUNG 2012). Bei Beaglen im Alter von 9 Wochen
trägt die Vorderextremität im Mittel 59,7% der Körpermasse, während es im Alter von
einem Jahr 63,5% sind. Damit überwiegen die Veränderungen der Rumpfform über
die übrigen morphometrischen Veränderungen und dominieren die Verschiebung der
Lage des CoM nach kranial. Ontogenetische Studien bei Säugetieren zum
Wachstum verschiedener Organe zeigten in Übereinstimmung mit einer kranialen
Verschiebung des CoM ein negativ allometrisches Wachstum von z.B. Niere und
Milz, während der Magen positive Allometrie zeigte (DEAVERS et al. 1972; LÜTZEN
et al. 1976; STEWART u. GERMAN 1999).
Die Verschiebung des CoM nach kranial ist aber nicht allein durch die Veränderungen
der Körperproportionen bedingt, sondern scheint auch durch posturale
Veränderungen hervorgerufen zu sein. Der posturale Index als Maß für das
Verhältnis von funktioneller zu anatomischer Beinlänge ermittelt aus der Länge des
Beines (von außen gemessen, vom Boden bis zum Widerrist bzw. Trochanter major)
im Stand geteilt durch die Summe der Länge der einzelnen Beinabschnitte
(BIEWENER 2003) zeigte beim Beagle v.a. für die Hinterextremität deutliche
Veränderungen. Wie auch bei Pferden (GROSSI u. CANALS 2010) wird beim Beagle
mit zunehmendem Alter die Hinterextremität gestreckter, und funktionelle und
anatomische Beinlänge nähern sich einander an. Umgekehrt heißt das, dass das
Hinterbein der jungen Hunde stärker flektiert ist. Aus der zunehmenden Streckung
der Hinterextremität resultiert ein Aufrichten der kaudalen Körperhälfte, welches
74

Diskussion
unweigerlich zu einer Verschiebung des Körpermasseschwerpunktes nach kranial
führt.
Im Unterschied zu den Befunden an Primaten liegt bei Hunden der CoM immer
relativ kranial, und diese Lage wird in der Ontogenese durch die Proportionsänderungen
verstärkt. Für verschiedene Primaten hat man, passend zur negativen
Allometrie des Kopfes, eine stärkere Änderung der Lage des Körpermasseschwerpunktes
beobachtet (Schimpansen, Japanmakaken: KIMURA 1987, 2000;
Rhesusaffen: TURNQUIST u. WELLS 1993; Totenkopfäffchen: YOUNG 2012). Hier
tragen die Vorderbeine über 50% des Körpergewichtes während des ersten
Lebensjahres, während der Körpermasseschwerpunkt bei adulten Tieren kaudal der
Körpermitte liegt und mehr als die Hälfte des Körpergewichtes auf den Hinterextremitäten
lastet. Bei den Jungbeaglen dagegen verlagert sich der Körpermasseschwerpunkt
zum einen nicht über die Körpermitte hinweg, und die beobachtete
Verschiebung erfolgt zum anderen in die entgegengesetzte Richtung. Ob sich ein
allgemeingültiges Muster dahinter verbirgt und sich bei Tieren, die als Adulti mehr als
50% des Körpergewichtes auf den Vorderbeinen tragen, der CoM während der
Ontogenese durchgehend weiter nach kranial verschiebt, bleibt offen, da bisher
ontogenetische Daten nur von Primaten und vom Beagle vorliegen. Darüber hinaus
wäre es interessant, die ontogenetischen Veränderungen der Lage des CoM bei
anderen Rassen mit deutlich abweichenden Körperbautypen zu untersuchen.
Als Intermediärtyp zwischen Platzhockern und Laufjungen sind junge Hunde daran
angepasst, relativ früh in der Entwicklung mit dem Rudel umher zu ziehen. Bezogen
auf die Körpergröße ist die Umwelt für kleine Säugetiere und damit auch für
Jungtiere stärker strukturiert. Dieses verlangt von kleinen Tieren eine größere
Wendigkeit. Ein weiter kaudal liegender CoM wirkt sich biomechanisch vorteilhaft auf
die Wendigkeit aus (AEARTS et al. 2003), und daher könnte die relativ weiter
kaudale Lage des CoM bei Welpen einen Vorteil für deren Manövrierfähigkeit bieten.
Um allerdings sogenannte ‚kick-starts’ (AERTS et al. 2003; WALTER u. CARRIER
2011) zu vermeiden, ist eine insgesamt kraniale Lage des CoM von Vorteil, so wie er
bei den Hunden dieser Arbeit von Beginn an zu beobachten war.
75

Diskussion
Die zunehmende kraniale Lage des Körpermasseschwerpunktes während des
Wachstums geht einher mit einer zunehmenden Belastung der Vordergliedmaßen in
der Ontogenese des Hundes. Dies könnte ein Faktor sein, der zu skelettalen
Erkrankungen von Junghunden gerade an den Knochen der Vorderbeine, wie die
Ellbogengelenksdysplasie, beitragen kann. Darüber hinaus führen Aktivitäten wie
Treppen hinuntersteigen zu einer besonders hohen Belastung der Vordergliedmaßen,
da die Neigung zu einer noch stärkeren Verschiebung des CoM nach kranial
führt.
Ein leicht zu ermittelnder Indikator für die Entwicklung eines Junghundes ist das
Körpergewicht. Die Jungbeagle in dieser Studie nahmen in den ersten vier
Lebensmonaten intensiv an Gewicht zu. Am Ende der Studie hatte noch kein Hund
das Gewicht der Elterntiere erreicht. Aus dem Vergleich der Ergebnisse dieser Arbeit
mit denen anderer Studien (HAWTHORNE et al. 2004; SALOMON et al. 1999) lässt
sich vermuten, dass kleinere Zuchtlinien des Beagles schneller die Zeit der
intensiven Gewichtszunahme abschließen und auch ihr Endgewicht früher erreichen.
Innerhalb einer Rasse kann es also abhängig vom Endgewicht der Hunde
Unterschiede in den Entwicklungszeiträumen geben, wobei Hunde größerer Linien
wahrscheinlich mehr Zeit für das Wachstum benötigen. Eine Validierung dieser
Beobachtung ist durch zukünftige Studien an anderen Rassen mit verschiedenen
Zuchtlinien nötig.
Vergleicht man die Wurfgeschwister aus dieser Studie untereinander, so ähneln
sich die Wachstumskurven unabhängig vom individuellen Gewicht. Hier nahm weder
der Schwerste länger zu, noch erreichte der Leichteste die Endwerte der Studie
früher. Darüber hinaus blieb die Gewichts- und Größenreihenfolge unter den
Geschwistern über den gesamten Studienzeitraum gleich. Dies deckt sich mit den
Ergebnissen einer früheren Studie (WEISE 1964). Bei der Auswahl eines Welpen im
Alter von neun Wochen kann also die Größe der Elterntiere zusammen mit den
Größenverhältnissen der Geschwister untereinander hilfreich sein zur Beurteilung
der Endgrößen der verschiedenen Individuen.
Durch die vorgelegte Arbeit sind erste Referenzdaten für die morphometrische
Entwicklung des Beagles und den Einfluss der Proportionsverschiebungen auf die
76

Diskussion
Lage des CoM erhoben worden. Inwiefern es sich bei den hier beobachteten Mustern
um für Hunde allgemeingültige Befunde handelt, muss durch zukünftige Arbeiten
geprüft werden, die insbesondere weitere Würfe der Rasse Beagle und von Rassen
verschiedener Körperbautypen und Körpergrößen einbeziehen. Erst dann können
fundierte Vergleiche zwischen Rassen und Zuchtlinien angestellt werden. Dabei
sollten zukünftige Arbeiten auch die ersten neun Lebenswochen als die intensivste
Entwicklungsphase einschließen. Ganganalytisch bleibt zu prüfen, welche anderen
Größen, wie z.B. Parameter der Bewegungsabläufe, sich neben der Lage des CoM
durch die Verschiebungen der Körperproportionen verändern. Hier soll die
anstehende Auswertung der kinematischen Daten und ihre Integration mit den
bereits bestehenden Befunden Aufschluss geben. Eine umfassendere Datenlage, die
morphometrische und ganganalytische Aspekte integriert, wird weiterhin ontogenetische
Vergleiche zwischen Rassen, aber auch zwischen Säugetierarten ermöglichen.
Die Ergebnisse können für den Vergleich mit orthopädischen Wachstumspathologien
genutzt werden.
77

Zusammenfassung
5. Zusammenfassung
Daniela Helmsmüller
Die ontogenetische Entwicklung des Bewegungsapparates beim Beagle -
eine morphometrische und kinetische Analyse
Im Leben von Hunden als cursoriale Säugetiere spielt die Fortbewegung eine
große Rolle. Störungen in der Entwicklung des Bewegungsapparates während des
Wachstums sind zu vermeiden bzw. wenn möglich frühzeitig zu diagnostizieren und
therapieren. Ziel dieser Arbeit war es, die ontogenetische Allometrie von Hunden am
Beispiel des Beagles zu dokumentieren und die Lage des Körpermasseschwerpunktes
zu analysieren. Besonderes Augenmerk galt der Skapula in der morphometrischen
Analyse, als bislang in ontogenetischen Studien vernachlässigter, aber
lokomotorisch relevanter Vordergliedmaßenknochen.
In dieser longitudinalen Studie wurden sechs Beaglerüden aus einem Wurf von
der neunten postnatalen Woche bis zum Alter von einem Jahr regelmäßig
untersucht. Ihr Gewicht, ihre Körperproportionen und die Längen der einzelnen
Gliedmaßenknochen wurden allometrisch betrachtet. Für die Bestimmung der
Verteilung des Körpergewichtes zwischen den Gliedmaßen trabten die Hunde auf
einem Laufband mit vier integrierten Kraftmessplatten, das die Erfassung der
vertikalen Bodenreaktionskraft und der Bodenkontaktzeiten erlaubte.
Beim Vergleich der sich funktionell entsprechenden Vorder- und Hintergliedmaßenabschnitte
zeigten sich beim Hund Unterschiede zu früheren Befunden von
Säugetieren durch eine höhere positive Allometrie von Femur und Crus im Vergleich
zu den Werten von Skapula und Brachium. Relativ zur Gesamtlänge des Beines
nahmen Antebrachium, Femur und Crus zu, während die Autopodien an Länge
abnahmen. Durch ihre nahezu optimalen Längenverhältnisse der Gliedmaßenabschnitte
von 1:1:1 und aufgrund der konstanten relativen Länge des Brachiums kann
vermutet werden, dass Hunde früh in ihrer Ontogenese selbststabilisierende
Mechanismen verwenden. Das negative allometrische Wachstum des Rumpfumfan-
78

Zusammenfassung
ges und eine relative Zunahme der Rumpflänge gingen mit einer Änderung der
Rumpfform von zylindrisch beim Junghund zu einer deutlich konischeren Form beim
Adulten einher. Diese Veränderung, gepaart mit einer gestreckteren Hintergliedmaße
beim erwachsenen Hund sowie beschriebenen Allometrien der inneren Organe,
führte zu einer Verschiebung des Körpermasseschwerpunktes nach kranial. Die
relativ stärkere kaudale Lage des CoM bei Welpen könnte einen Vorteil für deren
Wendigkeit bieten, um allerdings sogenannte ‚kick-starts’ zu vermeiden, ist die
generell kraniale Lage des CoM bei Hunden von Vorteil. Die sich kontinuierlich
verändernden Gliedmaßenverhältnisse und auch die unterschiedliche Lage des
Körpermasseschwerpunktes zusammen mit weiteren auslösenden Faktoren können
ein Grund für orthopädische Probleme im Wachstum sein. Zur einfachen Überprüfung
des physiologischen Wachstums von Hunden bietet sich die Gewichtsentwicklung
an. Die Dauer bis zum Erreichen des Endgewichtes und der intensivsten
Gewichtszunahme scheint verglichen mit kleineren Beagle-Linien und anderen
Rassen vom Endgewicht abhängig zu sein, wobei schwerere Hunde längere Zeiten
benötigen. Die Größenverhältnisse unter den Beaglegeschwistern blieben über den
gesamten Messzeitraum gleich und unter den Geschwistern unterschieden sich
Zunahmezeiten nicht. Inwiefern es sich bei den hier beobachteten Mustern um für
Hunde allgemeingültige Befunde handelt, muss durch zukünftige Arbeiten geprüft
werden, die insbesondere Rassen verschiedener Körperbautypen und Körpergrößen
einbeziehen.
79

Summary
6. Summary
Daniela Helmsmüller
Ontogenetic development of the locomotor system of the Beagle - a morphometric
and kinetic analysis
Locomotion plays a significant role in the life of the dog as a cursorial mammal and
one essential prerequisite for this is a physiologically developed musculoskeletal
system. To ensure its proper functioning, abnormalities in its development should be
avoided or at least if possible diagnosed and treated at an early stage. It was hence
the aim of this study to document the ontogenetic allometry of Beagles, in example of
dogs in general, and to analyse the location of the centre of body mass during
growth. Heed was paid in this study to the scapula as a locomotory important but in
ontogenetic studies often neglected element of the forelimb.
In this longitudinal study, six male Beagle siblings were analysed regularly from
the ninth postnatal week until they reached one year of age. Their weight, body
proportions and the lengths of their individual limb bones were measured and the
results evaluated allometrically. To determine the body weight distribution and
thereby the craniocaudal location of the center of body mass, the dogs trotted on the
treadmill with four integrated force plates and the vertical ground reaction forces as
well as the stance duration ratios were determined.
Comparing the functionally analogous fore- and hindlimb segments, deviations
from previously reported patterns were observed, i.e., femur and crus showed a
stronger positive allometry than scapula and brachium. Relative to limb length,
antebrachium, femur and crus increased whereas manus and pes decreased in
length. Because dogs show a segment ratio of nearly 1:1:1 and the relative length of
the middle segment of the forelimb (i.e., the brachium) is constant during growth, it is
postulated that dogs use self-stabilizing mechanisms from early on. The negative
allometric growth of the trunk circumference and a relative increase in the trunk
length compared with body mass were accompanied by a change of the shape of the
80

Summary
trunk from a cylindrical shape in the puppy to a more conical shape in the adult dog.
These changes, together with the elongation of the hindlimbs due to postural
changes and the described allometries of the inner organs led to a net-cranial shift of
the center of body mass. In contrast to primates, the location of the center of mass
was always situated cranially. The more caudal position of the CoM in puppies could
be advantageous for their maneuverability; to avoid the risk of pitching, however, a
net-cranial location is beneficial. The changing limb proportions together with the shift
of the body’s center of mass and other triggering factors could be a cause for
orthopaedical problems in growing dogs. A good indicator for a dogs’ growth is its
weight development. Compared to smaller-bodied Beagle lines and other breeds, the
growth period to reach the final weight as well as the period of the most intensive
weight gain seems to depend on the final weight. Thereby, relatively heavier dogs
need more time for growth. The body size relationships amongst the Beagle siblings
remained unchanged during the study period and their duration of weight increase
did not differ. Whether the data collected in this study are representative for dogs
remains to be tested in future studies, which should include breeds of varying builds
and body sizes.
81

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96

Danksagung
8. Danksagung
Mein ganz besonderer Dank gilt Herrn Prof. Nolte für die Überlassung dieses
interessanten Themas und für die Möglichkeit, das hervorragend ausgestattete
Ganganalyselabor der Klinik für Kleintiere, Stiftung Tierärztliche Hochschule
Hannover zu nutzen.
Mein besonderer, herzlicher Dank gilt Frau PD Dr. Schilling für die interessante
Aufgabenstellung, ihre große Unterstützung, zahlreiche Anregungen bei der
Durchführung der Arbeit und ihr unermüdliches Engagement.
Außerdem möchte ich mich bei Frau Anders für die Hilfe bei den Messungen und
auch bei den Tierpflegern für die gute Betreuung der Studienteilnehmer bedanken.
Auch allen weiteren Mitarbeitern der Klinik danke ich für ihre Hilfsbereitschaft.
Bei allen Mitdoktorandinnen und Mitdoktoranden der Klinik und vor allem der
Ganganalyse möchte ich mich für eine super Zusammenarbeit und ein tolles Team
bedanken. Frau Fischer gerade in der Endphase sehr herzlichen Dank für den
Informationsfluss.
Danke, Ulrich, für die Hilfe bei den Graphiken und Geduld und Durchhaltevermögen.
Auch meiner Familie, besonders Möni für ihr Englisch, und Freunden danke ich
für die große Unterstützung in vielerlei Hinsicht.
97