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Aplexa Marmorata (Guilding, 1828) (Basommatophora: Physidae) - an Invasive Freshwater Snail in South Africa

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Aplexa Marmorata (Guilding, 1828) (Basommatophora: Physidae) - an Invasive Freshwater Snail in South Africa Aplexa marmorata (Guilding, 1828) (Basommatophora: Physidae) - an invasive freshwater snail in South Africa. By Pelisa Dana Submitted in fulfilment ofthe academic Requirements for the degree of . Master of Science in the Department ofBiology, University ofNatal Durban March 2000 ABSTRACT Invasions ofecosystems by alien species is a worldwide problem. Man, with his constant travelling, introduces organisms to places they have never occurred in before. The introductions may be accidental or deliberate. Some ofthe introduced organisms become invasive and some of these also beco~e pests: Two aquatic pulmonate snails, Physa acuta (physidae) and Lymnaea columella (Lymnaeidae), were introduced to South Africa probably through the aquarium industry in the 1940s and have now spread to most ofthe country's freshwater systems. A third invasive pulmonate, and second physid provisionally called Aplexa cf. marmorata, has recently been found in South African freshwaters. Comparison between A.. cf. marmorata found in Durban and P..acuta from Pietermaritzburg as an example ofthe genus Physa, confirmed that they belong to different genera and are therefore different species. Features compared were.the shell, radula, foot, mantle, male genitalia and sperm morphology. Aplexa cf. marmorata is characterized by its foot having a pointed posterior end with a dark mid-dorsal stripe while that of P. acuta does not have these features. The mantle edge ofA.cf. marmorata has short triangular dentations while that ofP. acuta has long finger-like projections. Aplexa cf. marmorata does not have an externally visible preputial gland whereas P. acuta does. The penis ofA.cf. marmorata has a lateral opening while that ofP. acuta has a sub-terminal outlet. TEM sections ofthe spermatozoon ofA.c£ marmorata showed that it has a maximum oftwo glycogen helices around the mid-piece while P. acuta is known to have three. A study ofthe population dynamics ofA.cf. marmorata in Durban showed it to produce three overlapping generations within a 14 month ~ ~ . period whereas P. acuta has been shown to produce as many as eight over a similar time period. Further comparisons between South African A. cf. marmorata and similar material from the West Indies, Nigeria and St Lucia (KwaZulu-Natal) showed that they shared the same features with the specimens collected in Durban and are therefore considered to belong to the same species, Aplexa marmorata (Guilding, 1828). This species is indigenous to the Caribbean and northern parts of South America. The picture is however complicated by the fact that Dr L Paraense, doyen ofthe Brazilian school offreshwater malacology, does not recognize the genus Aplexa and redescribed this species under the name Physa marmorata in 1986. ii PREFACE The experimental work described in this dissertation was carried out in the Department ofBiology, University ofNatal, Durban, from June 1997 to July 1999, under the supervision ofProfessor C.C. Appleton. This study represents original work by the author and has not otherwise been submitted in any form for any degree or diploma to any tertiary institution. Where use has been made ofthe work ofothers, it is duly acknowledged in the text. Hi ACKNOWLEDGEMENTS I would like to thank my supervisor, Professor CC Appleton, for his guidance, encouragement, support, patience and advice throughout this study, without which this work would not have been possible. Thanks are also due to many other people: Dr Glenda Mathews (Department ofStatistics, University ofNatal) and Khangelani Zuma (Biostatistician, SA Medical Research Council) for their assistance with statistical analysis ofthe sampling data; The staffofthe Electron Microscope Unit (University ofNatal, Durban), Dr Fiona Graham and Ms Priscilla Maartens, for their assistance with the Scanning and Transmission Electron Microscopy ofthe snail tissues respectively; Vasi Muthusamy and her staffin the Histopathology Laboratory (University ofNatal Medical School) for assistance with the preparation ofhistological sections ofsnail tissue and to Dr Vivienne Chrystal (Department ofPathology, University ofNatal Medical School) for help in interpreting the sections; TheEnvironmental Health section ofthe Durban Metro Health Department and Mr Gerald Ncgobo (University ofNatal) for assistance with transport and sampling in the field; The Department ofGeographical & Environmental Sciences (University ofNatal) for preparing maps ofthe sampling localities; Dra Silvana Thiengo & Dr Lobato Paraense (Istituto Oswaldo Cruz, Rio de Janeiro, Brazil, and Dr J-P Pointier (Universite de Perpignan, France) for examining specimens ofAplexa cf. marmorata and giving their opinions on its identity; Dr M Glaubrecht (Berlin Museum, Germany) for providing the six shells ofPhysa mossambiquensis on loan; iv The Foundation for Research Development (now the National Research Foundation), Pretoria, and the University ofNatal Research Fund for financial support. Finally I would like to.thank my family, my friends and my colleagues for believing in me and for their encouragement when things were tough. v DEDICATION This work is dedicated to my son, Siko Ntando, who understood when I left him home to study. v LIST OF CONTENTS Page ABSTRACT ii PREFACE Hi ACKNOWLEDGEMENTS iv DEDICATION vi LIST OF CONTENTS vii LIST OF TN:JLES xi LIST OF FIGURES xii CHAPTER 1: Freshwater snails as invaders in Southern Africa 1 1.1 Definition ofan invasive organism 1 1.2 Biological invasions 4 1.3 How are invaders introduced? 6 1.4 The South African situation 6 ~~ 1.5 Objectives 7 1.5.1 General objective 7 1.5.2 Specific objectives 7 CHAPTER 2: Aquatic pulmonates as invaders 8 2.1 Intfoduction 8 2.2 The pulmonate radula 8 2.3 Eggs and egg capsules 9 2.4 Lymnaea columella (Say, 1817) (Lymnaeidae) 10 2.5 Physa acuta (Drapanaud, 1805) (Physidae) 11 vii CHAPTER 3: The family Physidae in Africa 12 3.1 Introduction 12 3.2PhysaDrapanaud,1801 12 3.2.1 Distribution 12 3.2.2 Shell 13 3.2.3 Mantle and foot 13 3.2,4 Male genitalia 13 3.2.5 Eggs 13 3.3 Aplexa Fleming, 1820 14 3.3.1 Distribution 14 3.3.2 The shell 14 3.3.3 Mantle and foot 14 3.3,4 Male genitalia 15 3.3.5 Eggs 15 3,4 Distinguishing South African Aplexa cf. marmorata from Physa acuta 15 3.5 Genital anatomy and shell shape ofphysids from Africa and the Caribbean 17 3.5.1 ~ptroduction 17 3.5.2 Materials and methods 17 3.5.3 Results 20 3.6 Conclusions 20 CHAPTER 4: What is Aplexa cf. marmorata'l 23 4.1 Historical account 23 4.2 Characterisation ofAplexa cf. marmorata from South Africa 25 4.2.1 Materials and methods 25 4.2.2 The shell 26 viii 4.2.3 The radula 26 4.2.4 The foot 29 4.2.5 The mantle 29 4.2.6 The penial complex 29 4.2.7 Sperm morphologyy 32 i) Scanning Electron Microscope 32 ii) Trans~ission Electron Microscope 33 4.2.7.1 Acrosome 38 ·4.2.7.2 The nucleus 38 4.2.7.3 The midpiece 38 i) Neck Region 38 ii) The glycogen helix region 38 a) Double helix region 43 b) Single helix region 43 c) Mitochondrial derivative region 43 4.2.7.4 Glycogen piece 43 4.2.7.5 End piece 47 4.3 Egg capsules 47 4.4 Identification 47 4.5 What is Physa mossambiquensis Clessin, 1886? 50 4.6 Conclusion 53 CHAPTER 5: Population fluctuations of Aplexa marmorata in South Africa 56 5.1 Introduction 56 5.2 Materials and methods 56 5.2.1 Botanic Gardens site 56 ix 5.2.2 BluffNature Reserve 59 5.2.3 Sampling technique 59 5.2.4 Temperature, pH and conductivity 59 5.2.5 Statistical analysis 62 5.3 Results 62 5.3.1 Botanic Gardens site 62 5.3.2 BluffNature Reserve site 68 5.3.3 Other freshwater snails 76 5.4 Discussion 78 CHAPTER 6: General discussion 82 REFERENCES -8 7 APPENDIX 1: Sectioning and staining ofthe snail's penial complex 101 APPENDIX2: Mucin staining technique 102 APPENDIX 3: Cleaning ofshell 103 APPENDIX 4: Extraction ofradula 104 APPENDIX 5: Scanning Electron Microscope protocol 105 APPENDIX 6: Transmission Electron Microscope protocol 106 ; ~ APPENDIX 7: Karyotype Protocol 107 APPENDIX 8: Percentage histograms for the BluffNature Reserve site 109 APPENDIX 9: Percentage histograms for the Botanic Gardens site 121 x /- LIST OF TABLES Table I: Differences between Physa marmorata and Physa cubensis. 54 Table 2: Differences between spermatozoa ofA. cf. marmorata and Physa acuta 55 Table 3: Temperature, conductivity, pH and turbidity at Botanic Gardens site 67 Table 4: Temperature, conductivity, pH and turbidity at BluffNature Reserve site 69 Table 5: Population density ofAplexa cf. marmorata at BluffNature Reserve 72 Table 6: Population density or'Aplexa cf. marmorata at Botanic Gardens 75 Table 7: Species composition and density at Botanic Gardens 77 (. xi LIST OF FIGURES Figure 3.1: Smooth and glossy shell ofA. cf. marmorata 16 Figure 3.2: Mantle dentations ofA. cf. marmorata 16 Figure 3.3: Penis ofA. cf. marmorata 18 Figure 3.4: Penis ofPhysa acuta 18 Figure 3.5: Reproductive system ofA. cf. marmorata 19 Figure 3.6: Shells from Guadeloupe and West Indies 21 Figure 3.7: Shells from Nigeria and St.Lucia, KwaZulu-Natal 21 Figure 3.8: Shells from Botanic Gardens and BluffNature Reserve 22 Figure 4.1: Radula ofA. cf. marmorata 27 Figure 4.2: Central teeth ofradula 27 \i. Figure 4.3: Newly formed, newly formed working, worn-out and normal teeth 28 Figure 4.4a: X-section through preputium ofA. cf. marmorata 30 Figure 4.4b: X-section through penial complex ofPhysa acuta 30 Figure 4.4c: Line drawing ofX-section through preputium ofA. cf. marmorata 32 Figures 4.5 & 4.6: Heads ofspermatozoa ofA. cf. marmorata 34 ! .•; Figures 4.7 & 4.8: Heads and double glycogen helices ofA. cf. marmorata 35 xii Figure 4.9: Annular ring on sperm tail 36 Figure 4.10: Tip ofspermatozoon tail 36 Figures 4.11 & 4.12: Coiled tail tip of spermatozoon 37 Figure 4.13a: Line diagram ofwhole mature spermatozoon of A.cf.
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