Aspects of the Reproductive Biology of Sengis (Macroscelidea) in general and the Postnatal Development of the Short-eared Sengi (Macroscelides proboscideus) in particular




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Aspects of the Reproductive Biology of Sengis (Macroscelidea) in general

and the Postnatal Development of the Short-eared Sengi (Macroscelides proboscideus) in particular

Inaugural-Dissertation

zur Erlangung des Doktorgrades Dr. rer.nat.

des Fachbereiches Biologie und Geographie

an der Universität Duisburg-Essen

Vorgelegt von



Gea Olbricht

aus Leipzig

Juli 2009

Die der vorliegenden Arbeit zugrunde liegenden Experimente wurden im Zoologischen Garten der Stadt Wuppertal, im Zentralafrikanischen Museum Tervuren, Belgien, im Museum Alexander Koenig, Bonn und in der Anatomischen Anstalt der Universität München, sowie in den südafrikanischen Museen McGregor in Kimberley und Amathole in King Williams Town durchgeführt.



1. GUTACHTER:

Prof. Dr. H. Burda, Universität Duisburg-Essen



2. GUTACHTER:

Prof. Dr. B. Sures, Universität Duisburg-Essen



3. GUTACHTER:

Dr. R. Asher, Universität Cambridge, GB



VORSITZENDER DES PRÜFUNGSAUSSCHUSSES:

Prof. Dr. D. Hering, Universität Duisburg-Essen



Tag der Disputation:

03. 07. 2009

When we try to pick anything for itself,

then it turns out that it is linked to everything else in the universe.



John Muir

Was wir wissen, ist ein Tropfen;

was wir nicht wissen, ein Ozean.

Isaac Newton

Es ist nicht schwer zu komponieren.

Aber es ist fabelhaft schwer,

die überflüssigen Noten unter den Tisch fallen zu lassen.



Johannes Brahms


Meiner Familie gewidmet,

Dr. Alexander Sliwa mit Leona, Feline und Olivia



ACKNOWLEDGMENTS

Six years came and went in the blink of an eye. Through it all, I´ve had a great deal of fun and it is a great pleasure for me to acknowledge all those who´ve helped me in this endeavour. In 2002 I approached Professor Hynek Burda of the Department of General Zoology at the University of Duisburg-Essen with the idea of initiating a study on the reproductive biology of sengis after I have had the unique opportunity of observing short-eared sengis during my time as curator at Wuppertal Zoo. It occurred to me that it was time to start a serious data collection on this amazing little creature beyond of some anecdotal information which I had noted from time to time. Prof. Burda as a small mammal specialist has always been fascinated by these unusual animals and he agreed to supervise this project. I thank him for all the advice, friendship and interest that I received from him.

But first of all, my husband Dr. Alexander Sliwa deserves very special thanks for encouraging me to start this research project, providing active and moral and support and for having put up with me during my dissertation. Being an ambitious zoologist too, he inspired me many times with useful ideas in the course of numerous discussions, reviewed some early drafts and helped to design various illustrations. He followed my research progress with big interest and reported some valuable information.

At the same time I would like to thank my parents, Drs. Franz and Adelheid Olbricht, who always motivated me to fight my way through, gave emotional support and helped with the children.

Wuppertal Zoo provided me with generous access to my study animals, the sengis, and I would like to extend my sincerest thanks to Dr. Ulrich Schürer and his staff. Especially, the keepers of the Great Apes Department and the Felid Department were always there to advise me and provided me with valuable details of sengi husbandry and additional information on my study animals during my absence. From these departments I obtained a large number of deceased specimens. Here again my husband as the former curator at Wuppertal Zoo, Zoo veterinarian Dr. Arne Lawrenz and curator André Stadler were excellent supporters in terms of communication and technical support. I had the invaluable opportunity to share the zoo´s data bank for sengis since 1976.

I am most grateful to Beryl Wilson, collection manager of the McGregor Museum in Kimberley, South Africa who shared her experience on sengis in the field with me and the data on various sengi species in the museum collection. Together with Lucas Thibedi of the Amathole Museum in King William´s Town, South Africa, she measured some specimens available in their collections. I am also grateful to Dr. Gustav Peters of the Zoological Institute and Museum Alexander Koenig, Bonn, Germany, Wim Wendelen of the Department African Zoology of the Royal Museum for Central Africa in Tervuren, Belgium and Dr. Siegfried Czernay and Jutta Heuer of Halle Zoo, Mr. Andreas Filz of Tierpark Bernburg, and Roy Bäthe from Erfurt Zoo, all Germany, for access to their collections or donations of specimens. The Natural History Museum of the Humboldt University Berlin greatly contributed by donating a female Petromus typicus which was crucial to define the position of dorsal teats. I thank Christine Bartos and the staff from the sengi department at Philadelphia Zoo for the good communication regarding data for Rh. petersi. I gratefully acknowledge the skillful help in preparing and staining the histological sections by Astrid Sulz from the Institute for Anatomy, University of Munich. Rebecca Banasiak from the Field Museum of Natural History in Chicago, USA, provided the schematics of Figs. 2.1 and 3.1 and constructed Fig. 3.2 based on photographs.

I am greatly indebted to the following scientists and the co-authors of publications which will derive from the data of this thesis. Prof. Mike Perrin of the University of KwaZulu-Natal, Pietermaritzburg, RSA, Dr. William Stanley from the Field Museum of Natural History in Chicago, USA, Prof. Ulrich Welsch from the Institute for Anatomy, University of Munich, Dr. Robert Asher from the Museum of Zoology at the Cambridge University, UK, who provided additional information and advice for various aspects of the manuscript. With their scientific experience and enthusiasm they were highly supportive. Also special thanks to Dr. Galen Rathbun of the California Academy of Sciences, San Francisco, USA, and to Klaus Rudloff, curator at Tierpark Berlin-Friedrichsfelde, for the inexhaustible dialogue on the Afrotheria in general and sengis in particular.

So many others have helped with the work or just helped to keep me sane. To all the graduate students in the Department of General Zoology of the University Essen-Duisburg: thanks for all the good times and all the help they have given me over the years. In particular, Dr. Sabine Begall was always there to be of assistance with statistic and special questions or just to relax my mind in times of frustration. Together with Dr. Regina Moritz she was also a never dwindling source for providing scientific articles and good spirits



LIST OF CONTENTS

ACKNOWLEDGEMENTS

I SUMMARY — 1

II ZUSAMMENFASSUNG — 3

III GENERAL INTRODUCTION — 5

III.1 Fossil and extant macroscelids — 5

III.2 Afrotheria - hypothesis in mammalian evolution? — 6

III.3 Testicond afrotheres — 7

III.4 Molecular versus morphological research — 7

CHAPTER 1

1. REPRODUCTIVE PATTERNS OF SENGIS (MACROSCELIDEA) – A THEORETICAL APPROACH — 9

1.1 Abstract — 9

1.2 Introduction — 9

1.2.1 Aim of the study — 10

1.3 Material and Methods — 12

1.4 Results — 12

1.5 Discussion — 15

1.5.1 Placentation in afrotheres — 16

1.5.2 Developmental status at birth — 16

1.5.2.1 Environmental factors influencing the developmental status of birth

—17

1.5.2.2 Development of precociality — 17



1.5.2.3 Precocial and altricial strategies — 18

1.5.3 Gestation length — 19

1.5.4 Parental care — 19

1.5.4.1 Lactation — 20

1.5.4.2 Feeding intervals — 20

1.5.5 Monogamy — 20

1.5.5.1 Monogamy and parental care — 21

1.5.5.2 Mate guarding — 21

1.5.5.3 Monogamy and precociality — 22

1.5.6 Juvenile mortality — 22

1.5.7 Litter size — 23

1.5.7.1 Correlation between teat number and litter size — 23

1.5.7.2 Limits of litter size — 24

1.5.8 Seasonality of breeding periods — 25

1.5.8.1 Male capacities — 26

1.5.9 Post-partum oestrous — 26

1.5.10 Poly-ovulation — 26

1.5.10.1 Female capacities — 27

1.5.11 Longevity and fecundity — 27

1.6 Conclusions — 28



CHAPTER 2

2. THE TOPOGRAPHIC POSITION OF THE PENIS IN SENGIS (MACROSCELIDEA); AND COMMENTS ON PENIS TOPOLOGY IN TESTICOND MAMMALS — 32

2.1 Abstract — 32

2.2 Introduction — 32

2.2.1 Sengis as testicond afrotheres — 33

2.1.2 Taxonomic tools — 33

2.1.3 Aim of the study — 34

2.2 Material and Methods — 34

2.2.1 Material — 34

2.2.2 Methods — 34

2.2.2.1 Hyracoidea — 35

2.2.2.2 Statistical methods — 36

2.3 Results — 36

2.3.1 Sengi measurements — 36

2.3.2 Hyrax accounts — 39

2.4 Discussion — 39

2.4.1 Distance anus-penis — 39

2.4.2 Genital morphology in the Afrotheria — 40

2.4.3 Copulation posture — 40

2.4.4 Hyracoidea — 41

2.5 Conclusions — 41



CHAPTER 3

3. THE TAXONOMIC DISTRIBUTION OF MAMMARY GLANDS IN SENGIS — 42

3.1 Abstract — 42

3.2 Introduction — 42

3.2.1 Nomenclature of teat positions — 43

3.2.2 Behavioural ecology — 44

3.2.3 Aim of the study — 44

3.3 Material and Methods — 44

3.3.1 Material — 44

3.3.2 Methods — 44

3.4 Results — 46

3.4.1 Locations of the mammae — 46

3.4.1.1 Males — 46

3.4.1.2 Females — 47

3.4.1.3 Formulas — 51

3.5 Discussion — 52

3.5.1 Teats on male sengis — 52

3.5.2 Teats on female sengis and formulas — 53

3.5.3 The enigma about nuchal, lateral and dorsal teats — 54

3.5.3.1 Historical observations — 54

3.5.3.2 The presence of dorsolateral teats — 54

3.5.3.3 Defining a dorsolateral teat location — 55

3.5.3.4 Functionality of teats — 55

3.6 Conclusions — 56

CHAPTER 4

4. HISTOLOGICAL AND HISTOCHEMICAL STUDY OF THE MAMMARY GLANDS OF PETRODROMUS TETRADACTYLUS — 57

4.1 Abstract — 57

4.2 Introduction — 57

4.2.1 Mammae in male mammals — 58

4.2.2 Aim of the study — 58

4.3 Material and Methods — 59

4.3.1 Material — 59

4.3.2 Methods — 59

4.3.2.1 Fixation, embedding and staining methods — 59

4.3.2.2 Histochemistry of lectins — 60

4.4 Results — 60

4.4.1 General findings (light microscopy) — 60

4.4.1.1 Females — 60

4.4.1.2 Males — 60

4.4.2 Specific histological and histochemical findings — 61

4.4.2.1 Female mammary gland — 61



Actin — 61

PAS reaction — 61

Alcian blue — 62

Lectins — 63

4.4.2.2 Male mammary gland — 65



Lectins — 65

4.4.2.3 Scent glands — 67

4.5 Discussion — 69

4.5.1 Histo-morphology of mammary glands in Petrodromus — 69

4.5.2 The presence of mammae in male sengis — 69

4.5.3 Other glands — 70

4.6. Conclusions — 71

CHAPTER 5

5. BODY METRICS OF THE SHORT-EARED SENGI (MACROSCELIDES PROBOSCIDEUS, SMITH 1829) — 72

5.1 Abstract — 72

5.2. Introduction — 72

5.2.1 Body metrics and other physical patterns — 73

5.2.2 Growth models — 73

5.2.3 Aim of the study — 74

5.3 Material and Methods — 74

5.3.1 Material — 74

5.3.2 Methods — 74

5.3.3 Statistical analysis — 75

5.3.3.1 The Gompertz growth model — 76

5.4 Results — 76

5.4.1 The Gompertz model — 76

5.4.2 Sexual dimorphism — 78

5.4.3 Correlation of body length with hind foot length and body mass — 79

5.5 Discussion — 80

5.5.1 Measuring scheme and statistical methods — 80

5.5.2 Sexual dimorphism — 81

5.5.3 Developmental stage at birth and mating system — 81

5.5.4 Growth patterns and maturity — 82

5.5.4.1 The Gompertz growth parameters — 82

5.5.4.2 Body length against hind foot length and body mass — 82

5.5.4.3 Factors influencing precociality — 83

5.5.4.4 Lactation — 84

5.5.4.5 Skeletal growth and sexual maturity — 85

5.6 Conclusions — 85



CHAPTER 6

6. POST-NATAL BODY MASS DEVELOPMENT OF THE SHORT-EARED SENGI (MACROSCELIDES PROBOSCIDEUS) — 86

6.1 Abstract — 86

6.2 Introduction — 86

6.2.1 Growth models — 86

6.2.2 Aim of the study — 87

6.3 Material and Methods — 87

6.3.1 Material — 87

6.3.2 Methods — 87

6.3.2.1 Gompertz growth model and statistics — 88

6.4 Results — 88

6.4.1 Growth curves — 88

6.4.2 Gompertz growth parameters — 89

6.4.2.1 Sex-specific growth — 90

6.5 Discussion — 91

6.5.1 Environmental and behavioural impact on weight development — 91

6.5.2 Growth parameters — 92

6.5.3 Adult body mass — 93

6.5.3.1 Estimated adult weight — 93

6.5.3.2 Relating body mass to sexual maturity — 94

6.5.3.3 Sexual dimorphism — 94

6.6 Conclusions — 94

IV REFERENCES — 95

V APPENDIX — 110

A List of tables — 110

B List of figures — 111

C Staining procedures — 112

D Table: Raw data on individual body measurements of male and female Macroscelides

proboscideus — 115

E Vita — 118

F Liste der Veröffentlichungen — 120

I SUMMARY

Sengis have been studied for more than a century but information on their biology is still scattered. The reproductive biology of sengis is best understood in the context of their evolutionary history. Their phylogeny has long been the subject of much speculation and controversy. This thesis aims to consolidate molecular findings of other studies with morphological methods and thus, to contribute to a better understanding of their phylogeny. Sengis are members of the Afrotheria, an African clade of mammals, and particular attention was paid in this study to their relationships to other afrotheres.

Chapter 1 summarizes the knowledge on reproductive parameters across the order Macroscelidea from the literature. Various reproductive characteristics are unusual for a small mammal. The most important traits in the life history of sengis in terms of reproduction are precociality and monogamy as well as the ability of some species to poly-ovulate and to perform post-partum oestrus. Further, they have a very long lifespan with high fecundity rates.

In chapters 2 and 3 I apply morphological methods to investigate phylogenetic relationships. Morphological landmarks such as the position of penis and teats were defined. The position of the penis is of utility in distinguishing between the genera Petrodromus and Macroscelides, but not between any other genera of sengi, supporting recent taxonomic conclusions regarding the relationship of these two taxa. Teat position is useful in taxonomic distinction among the three of the four genera, only between Macroscelides and Elephantulus there was no difference. Only in two species teats were found on males: Elephantulus rozeti and Petrodromus tetradactylus but not on other species examined. This supports the recent taxonomic conclusions regarding the relationship of these two taxa. The arrangement of teats was determined in a formula for each genus which distinguishes between antebrachial, abdominal and inguinal regions. No sengi exhibited teats situated dorsolaterally to the extent of those in rock-dwelling mammals such as Petromus typicus.

In chapter 4 mammary tissue of a female and male P. tetradactylus was examined with different histological and histochemical methods. The results reveal a potentially functioning mammary gland in male Petrodromus with evidence of active mammary tissue. The secretory units (acini) are sexually dimorphic. In the female typical acini, milk ducts, cisternal milk sinus and a teat canal can be distinguished. The acini of the females occur in the periphery of the gland whereas acini in the male teat occur in the connective tissue of the teat. The function of mammary tissue in male Petrodromus is not clear because males of none of the sengi species contribute to the raising of their young. Apocrine scent glands were found in both genders at the base of the teat which underlines the importance of chemical communication for sengis.

In chapter 5 body measures (mass, length of body, head, ear, snout, whiskers, tail, hind foot) of captive short-eared sengis (Macroscelides proboscideus) were taken post mortem and then fitted to the 3-parameter Gompertz model There was considerable variation of the growth parameters of these body measures in terms of growth constant (K) and inflection age (I). Whiskers and snout had the fastest growth, the ears the slowest. The asymptotic value of the growth model (A) in terms of adult length of tail and ear as well as body mass was exceeded later then the sigmoidal curves suggested but nevertheless, adult size of all body parts is achieved at about sexual maturity (ca. 45 days), except hind foot length which reached its maximum earlier. No significant sexual dimorphism in the estimated adult size could be determined.

Chapter 6 refines the results regarding body mass growth during the ontogeny of individual short-eared sengis which were weighed on a nearly daily basis from their first days of life until adulthood. The Gompertz growth model was used to generate the growth parameters K, I and A which were compared with data on the reproductive biology of sengis. Furthermore, the growth parameters for Macroscelides were compared with those of various species obtained from the literature.Adulthood is reached when adult size matches with sexual maturity, at about 45 days. There were no significant differences between males and females in growth or adult body mass size.

II ZUSAMMENFASSUNG
Rüsselspringer oder Elefantenspitzmäuse (Macroscelidea) werden seit mehr als einem Jahrhundert wissenschaftlich untersucht, jedoch sind Informationen zu ihrer Biologie lückenhaft und zusammenhanglos. Die Fortpflanzungsbiologie von Rüsselspringern wird am besten im Kontext zu ihrer Evolutionsgeschichte verständlich. Ihre Phylogenie war lange Gegenstand von Spekulationen und Kontroversen. Diese Arbeit hat zum Ziel, Erkenntnisse aus der Molekulargenetik mit morphologischen Methoden zu unterstützen und somit zu einem besseren Verständnis ihrer Stammesgeschichte beitragen. Rüsselspringer gehören zu den Afrotheria, einer Gruppe von endemischen afrikanischen Säugetieren. Diese Verwandschaftsbeziehungen fanden hier besondere Berücksichtigung.

Kapitel 1 faßt das bisherige Wissen über Aspekte der Fortpflanzungsbiologie der Ordnung Macroscelidea zusammen. Einige Charakteristika sind für Kleinsäuger ungewöhnlich. Zu wichtigen Reproduktionsparametern zählt, dass Rüsselspringer Nestflüchter sind und monogam leben. Daneben sind einige Arten zu Polyovulation und post-partum- Östrus befähigt. Während ihrer relativ langen Lebensdauer erreichen sie eine bemerkenswerte Geburtenrate.

In den Kapiteln 2 und 3 wandte ich morphologische Methoden zur Untersuchung phylogenetischer Verwandschaftsbeziehungen an. Morphologische Meßpunkte wie die Position von Penis und Zitzen wurden festgelegt. Die Position des Penis diente der Unterscheidung der Gattungen Petrodromus und Macroscelides, jedoch nicht zu oder zwischen den anderen Gattungen. Dieses Ergebnis bestätigt neuere taxonomische Schlussfolgerungen zur weniger engen Verwandtschaft dieser beiden Taxa. Die Lage der Zitzen führte zur taxonomischen Unterscheidung von 3 der 4 Gattungen, zwischen Elephantulus und Macroscelides besteht kein bedeutsamer Unterschied. Nur bei den beiden Arten Petrodromus tetradactylus und Elephantulus rozeti wurden beim Männchen Zitzen gefunden, was Ergebnisse neuerer Untersuchungen zur engen Verwandschaft dieser beiden Taxa bestätigte. Die Anordnung der Zitzen definierte ich für alle 4 Gattungen in einer gattungsspezifischen Formel, wobei zwischen antebrachialer, abdominaler und inguinaler Position unterschieden wurde. Kein Rüsselspringer zeigte dorsolaterale Zitzen, wie sie bei der Felsenratte (Petromus typicus) bekannt sind.

Das Milchdrüsengewebe einer männlichen und weiblichen Rüsselratte (P. tetradactylus) wurde mit verschiedenen histologischen und histo-chemischen Methoden in Kapitel 4 untersucht. Die Egebnisse ergaben beim Männchen eine funktionsfähige Milchdrüse mit aktivem Milchgewebe. Die Drüsenendstücke unterschieden sich geschlechtsspezifisch. Beim Weibchen fanden sich typische Drüsenendstücke, Milchgänge sowie Milchsinus und Zitzenkanal. Die Drüsenendstücke des Weibchens befanden sich in der Drüsenperipherie, die des Männchens im Bindegewebe der Zitze. Die Funktion von Milchdrüsengewebe bei der männlichen Felsenratte bleibt unklar, da sich bei keiner Rüsselspringerart die Männchen an der Jungenaufzucht beteiligen. Apokrine Duftdrüsen wurden bei beiden Geschlechtern an der Zitzenbasis gefunden, was die große Bedeutung der olfaktorischen Kommunikation für Rüsselspringer unterstreicht.

Die Kapitel 5 und 6 beschäftigen sich mit post-natalem Wachstum. In Kapitel 5 wurden Körpermaße wie die Längen von Kopf-Rumpf, Ohr, Schnauze, Fibrissen, Schwanz und Hinterfuß sowie das Körpergewicht post-mortem bei zoogeborenen Kurzohr-Rüsselspringern (Macroscelides proboscideus) verschiedenen Alters vermessen und mit Hilfe des Gompertz-Wachstumsmodells analysiert. Dabei konnten erhebliche Unterschiede beim Wachstum der verschiedenen Körpermaße im Hinblick auf die Wachstumskonstante (K) und den Zeitpunkt des schnellsten Wachstums (I) festgestellt werden. Bei Fibrissen und Schnauze konnte generell das schnellste Wachstum verzeichnet werden, beim Ohr das langsamste. Die Annäherung an die Asymptote (A) für die adulte Länge von Schwanz und Ohr, sowie für das Adultgewicht zeigte sich in Anwendung des Wachstumsmodells später als es der sigmoidale Kurvenverlauf der direkten Meßwerte vermuten ließ. Der Hinterfuß erreichte seine Adultlänge früher als die anderen Körperteile, für die Adultmaße ungefähr beim Einsetzen der Geschlechstreife (ca. 45. Lebenstag) ermittelt wurden. Keine Signifikanz konnte für geschlechtsspezifischen Dimorphismus der im Modell ermittelten geschätzten Adultmaße festgestellt werden.

Die tägliche individuelle Gewichtszunahme von zoolebenden Kurzohr-Rüsselspringern von den ersten Lebenstagen an bis ins Erwachsenenalter war Gegenstand der Untersuchung in Kapitel 6. Die Ergebnisse des vorherigen Kapitels konnten auf der Grundlage von kompletten Meßreihen der Gewichtsentwicklung überprüft und mit Hilfe des Gompertz-Modells analysiert werden. Die Wachstumsparameter K, I und A wurden mit Aspekten der Fortpflanzungsbiologie von Rüsselspringern in Zusammenhang gesetzt und konnten gleichzeitig mit den für andere Arten aus der Literatur bekannten gleichen Wachstumsparametern verglichen werden. Es gab keine signifikanten Unterschiede zwischen Männchen und Weibchen bezüglich Wachstum oder Adultmaß beim Körpergewicht. Das Ergebnis für das Erreichen des Adultgewichtes entsprach mit 45 Tagen dem Ergebnis des vorherigen Kapitels.



III GENERAL INTRODUCTION

The Macroscelidea is a monophyletic order with the family Macroscelidae which comprises 16 well defined species in two subfamilies (Rovero et al. 2008): the Macroscelidinae with the genera Petrodromus, Elephantulus and Macroscelides and the Rhynchocyoninae with the only genus Rhynchocyon.

The English name “elephant-shrew” originated because of the superficial similarities the Macroscelidea bear to other mammals, and in historical (and erroneous) taxonomic opinions. In particular, these animals have a very different evolutionary history than true shrews (Soricidae) and they share few life history traits. Because of this misleading nature of this name, authors (e.g. Rathbun and Woodall 2002, Skinner and Chimimba 2005) are increasingly using the African term “sengi” for elephant-shrew, which is derived from the Kiswahili word “sanje” (Eastern Africa, Rathbun and Kingdon 2006) or from the Lunda-word “Isengi” (Zambia, White and Ansell 1966). I agree with these scientists that it is appropriate to use local names and this protocol is followed here.

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