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A Thesis Submitted for the Degree of Master of Philosophy from the University of London and the Diploma of Membership of Imperial College

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TAXONOMIC STUDY OF THE BULINUS AFRICANUS GROUP IN KENYA BY RICHARD ARCHER A thesis submitted for the degree of Master of Philosophy from the University of London and the Diploma of Membership of Imperial College Department of Pure and Applied Biology, Imperial College, London SW7 and Experimental Taxonomy Unit, Department of Zoology, British Museum (Natural History), London SW7 5BD. 2 ABSTRACT Certain species of the Bulinus africanus group have been implicated in the transmission of Schistosoma haematobium in Kenya. Full taxonomic resolution of the group has previously been hampered by extensive intergradation of form between certain taxa. The major source of difficulty has been the inadequate quantification of traditional characters, particularly those on the shell. With the advent of various numerical and experimental techniques there is a need for re-assessment of shell morphology. This study involved the morphological characterisation of populations from Western and Central Kenya, using new and traditional shell variables. These were standardised and quantified morphometrically, producing two data sets: PI, consisting of four morphologically distinct samples; and P2, consisting of 10 larger samples, less visually distinct. PI and P2 were subjected to multivariate analysis, principally Canonical Variates Analysis and Principal Components Analysis. This study suggests that Principal Components Analysis is of limited use in resolving samples using shell variables. Canonical Variate Analysis is a more useful technique since it minimises the effects of variation within each sample whilst maximising variation between samples. Numerical analysis suggests the presence of three morphotypes among these samples, corresponding to the b.africanus^B.nasutus and B.globosus/ugandae forms. The effects of isometric and allometric growth are discussed. The most useful discriminatory variables appear to be the\anglessuet-c A, AAA, APA and BWSA. Other variables are discussed. Results from polyacrylamide gel isoelectrophoresis of four enzyme systems are also presented. These generally support the morphometric interpretation, as do the egg protein separations. A detailed description is given of shell microsculpture in the Bulinus africanus group in Western Kenya. Details of the parasite burdens of the wild caught snails are also documented. pftfrS: C O N T E N T S H C H A P T E R 1 INTRODUCTION 1! 1.1 GENERAL INTRODUCTION 14 1.2 T H E Bulinus africanus G R O U P IN K E N Y A IS 1.3 HISTORICAL PERSPECTIVE TO THE STUDY O F Bulinus n M PRESENT RESEARCH AND PROBLEMS 2.1 C H A P T E R 2 HISTORY OF CHARACTERS USED IN THE TAXONOMY OF BULINUS LI 2.1 SHELL MORPHOLOGY IS 2.2 ANATOMICAL CHARACTERS 17 2.3 BIOCHEMICAL CHARACTERS 31 2 M PARASITOLOGICAL STUDIES 31 2.5 ECOLOGICAL, BEHAVIOURAL AND PHYSIOLOGICAL STUDIES 34 CHAPTER 3 MATERIALS AND METHODS 34 3.1 SNAIL CAPTURE, MAINTAINANCE AND PRESERVATION 34 (a) DETAILS OF PRESERVED MATERIAL AND FIELD COLLECTION 3 C> (b) FIELD CAPTURE AND PRESERVATION 3T ( c) LABORATORY MAINTAINANCE 3<1 (d) SCHISTOSOME EXTRACTION 34 (e) CLEANING AND PREPARATION OF PRESERVED SHELLS 34 (f) EXAMINATION OF SHELLS 4 0 ' (g) SHELL ORIENTATION 3.2 NUMERICAL ANALYSIS 4fc (a) INTRODUCTION 4 (o (b) PRELIMINARY ANALYSIS Pi 4fe (1) CHOICE OF VARIABLES 46 (2) NUMBER OF INDIVIDUALS MEASURED W (3) ASSESSMENT OF ALLOMETRY 4* (4) MULTIVARIATE ANALYSIS 4? ( i) ORDINATION/MULTIDIMENSIONAL SCALING (ii) HIERARCHICAL CLUSTERING S3 ( c) MAIN ANALYSIS P2 4 PAGE : Sty 3.3 BIOCHEMICAL ANALYSIS 54- (a) ISOELECTRIC FOCUSING (IEF) 54- (1) INTRODUCTION St* (2) GEL PREPARATION AND RUNNING A SYSTEM 5 2 (b) EGG PROTEIN ELECTROPHORESIS s<\ 3.4 SCANNING ELECTRON MICROSCOPY c>\ C H A P T E R 4 RESULTS 61 4.1 MORPHOMETRIC ANALYSIS 61 A. PROGRAMME PI U (a) VISUAL INSPECTION OF SAMPLES M (b) ASSESSMENT OF ALLOMETRY 6>3 (c) UNIVARIATE AND BIVARIATE ANALYSIS 6>3 (d) PRINCIPAL COMPONENTS ANALYSIS CA (1) FULL DATA SET 11 (2) SIZE-EFFECT REMOVED 1 ( (3) REDUCTION IN NUMBER OF VARIABLES 15 (e) CANONICAL VARIATES ANALYSIS 1 5 (f) PRINCIPAL CO-ORDINATES ANALYSIS 2 1 (g) HIERARCHICAL CLUSTERING ANALYSIS B. PROGRAMME P2 W (a) VISUAL INSPECTION OF SAMPLES 84- (b) ASSESSMENT OF ALLOMETRY 98 (c) UNIVARIATE AND BIVARIATE ANALYSIS °1 0 (d) PRINCIPAL COMPONENTS ANALYSIS (1) FULL DATA SET 53 (2) SIZE-EFFECT REMOVED 13 (3) REDUCTION IN NUMBER OF VARIABLES <?3 (4) INCLUSION OF VARIABLES FROM 4TH & 5TH W H O R L S 55 (e) CANONICAL VARIATES ANALYSIS 5 PAO?E : 105 4*. 2. ISOELECTRIC FOCUSING ELECTROPHORESIS 105 (CL) ACID PHOSPHATASE 109 (b) MALATE DEHYDROGENASE 109 (c) GLUCOSE PHOSPHATE ISOMERASE |0<f W) HYDROXYBUTYRATE DEHYDROGENASE us 4.3 EGG PROTEIN ELECTROPHORESIS IIS 4.4 PARASITOLOGY 120 4.5 EXAMINATION OF SHELL MICROSCULPTURE 130 CHAPTER 5 DISCUSSION 130 5.1 NUMERICAL DISCUSSION 132. 5.2 VARIABLE ASSESSMENT 133 5.3 ISOELECTROPHORESIS DISCUSSION m 5.4 EGG PROTEINS DISCUSSION 135 5.5 PARASITOLOGICAL DISCUSSION 13L 5.6 S U M M A R Y 13S ACKNOWLEDGEMENTS 139 REFERENCES 150 A P P E N D I X - 151 DATA FOR PRESERVED KENYAN MATERIAL PI PROGRAMME |57 DATA FOR COLLECTED FIELD MATERIAL 1985 P2PROGRAMME 6 Pflfrg: LIST OF FIGURES 12 FIG 1 - MAP OF KENYA IX 2 - MAP OF COASTAL LOCALITIES VISITED 12 3 - MAP OF COLLECTION LOCALITIES NEAR LAKE VICTORIA 15 4 - DISTRIBUTION O F TH E Bulinus afrlcanus G R O U P IN K E N Y A 2 4 5 - M A I N S H E L L FE A T U R E S O F Bulinus 41 6.1 - PLAN VIEW OF SHELL APEX THROUGH GRATICULE 4-1 6.2 - DETAIL OF WHORL MEASUREMENT 4*1 6.3 - POSITIONING OF WHORL ORIENTATED SHELL FOR DRAWING 41 6.4 - POINTS OF FOCUS (P & Q) FOR STANDARD SHELL ORIENTATION 4 2 7.1 - WOV: SHELL MEASUREMENTS USED IN PI AND P2 4 2 7.2 - WOV: FURTHER SHELL MEASUREMENTS USED IN PI AND P2 4 3 8.1 - AOV: LINEAR SHELL MEASUREMENTS USED IN PI AND P2 4 3 8.2 - AOV: ANGULAR SHELL MEASUREMENTS USED IN PI AND P2 4 5 8.3 - COLLUMELLAR VARIABLES USED IN PI AND P2 <o% 9 - REPRESENTATIVE SHELLS FROM THE FOUR PI SAMPLES: <oZ 9.1 & 9.2 A R A M M A R K E T Q>Z 9.3 <5c 9.4 MIWANI Q>Z 9.5 & 9.6 K A P S I M O T W A D A M Q>Z 9.7 - 9.9 KISUMU ABATTOIR fafa 10 - CORRELATION MATRIX OF PI VARIABLES £>g 11 - PI - PRINCIPAL COMPONENT PLOTS FOR FULL DATA SET: 11.1- PC I A G A I N S T P C 2 eg 11.2- PCI AGAINST PC2 - AREA OF DISTRIBUTION OF THE FOUR SAMPLES 61 11.3- PCI A G A I N S T PC 3 c* 11.4- PC2 AGAINST PC3 1 2 12 - PI - PRINCIPAL COMPONENT PLOTS FOR FULL DATA SET, WITH ISOMETRIC SIZE EFFECT REMOVED: 1 2 12.1- PC I A G A I N S T PC 2 1 3 12.2- PC I A G A I N S T PC 3 1 3 12.3- PC2 AGAINST PC3 l b 13 - PI - PRINCIPAL COMPONENT PLOTS FOR FULL DATA SET WITH 6 VARIABLES REMOVED: l b 13.1- PCI AGAINST PC2 n 13.2- P C I A G A I N S T PC 3 TT 13.3- PC2 AGAINST PC3 n 14 - PI - CANONICAL VARIATE ANALYSIS FOR FULL D/.TA SET: 11 14.1- CV1 AGAINST CV2 * 0 14.2- CV2 AGAINST CV3 % 0 14.3- CV1 A G A I N S T CV 3 PflCrE S3 FIG 15 - PI - PRINCIPAL COORDINATE PLOT AND MINIMUM SPANNING TREE. PCI AGAINST PC2 S3 16 - PI - HIERARCHICAL CLUSTERING DENDROGRAM (SINGLE LINKAGE) ?S 17 - REPRESENTATIVE SHELLS OF ADDITIONAL P2 SAMPLES : 17.1-17.4 B.africanus F O R M (C V A S A M P L E A) KISIAN S T R E A M SS- 17.5-17.8 B.nasutus F O R M (CVA S A M P L E S) KISIAN S T R E A M st 17.9 & 17.10 B.africanus FO R M , PA P O N D I T I St 17.11 & 17.12 B.africanus/nasutus FO R M , MIGOSI SI 17.13 & 17.14 B.(?)globosus F O R M , S H A M B A SI 17.15 & 17.16 B.(?)ugandae FORM, ASEMBO BA Y n 17.17 & 17.18 B.africanus/nasutus FO R M , KINYUI 18 - BIVARIATE PLOT SEPARATING THE TWO KISIAN STREAM MORPHOTYPES: UPPER SPIRE HEIGHT AGAINST SHELL LENGTH 19 - CORRELATION MATRIX OF P2 VARIABLES K 20 - P2 - PRINCIPAL COMPONENT PLOT FOR FULL DATA SET PCI AGAINST PC2 ONLY % 21 - P2 - PRINCIPAL COMPONENT PLOT FOR FULL DATA SET, WITH ISOMETRIC SIZE-EFFECT REMOVED PCI AGAINST PC2 ONLY W 22 - P2 - PRINCIPAL COMPONENT PLOT FOR FULL DATA SET, WITH 7 VARIABLES REMOVED. PCI AGAINST P C 2 O N L Y q s 23 - P2 - PRINCIPAL COMPONENT PLOT FOR OTUs WITH FULL DATA SET AND COMPLETE FOURTH AND FIFTH WHORL MEASUREMENTS. PCI AGAINST PC2 ONLY loz 24 - P2 - CANONICAL VARIATE ANALYSIS FOR FULL DATA SET. CV1 A G A I N S T CV 2 O N L Y 102- 25 - P2 - MAHALANOBIS DISTANCE DENDROGRAM (SINGLE - LINKAGE) FOR 11 SAMPLES u z 26 - DIAGRAMMATIC REPRESENTATION OF THE MAIN IEF BANDING PATTERNS: u z 26.1 A c P n z 26.2 MDH u z 26.3 GPI IIZ 26.4 HBDH • Pfl o e • i n FIG 27 - RELATIVE EGG PROTEIN BAND INTENSITY PROFILES AND CELLULOSE ACETATE STRIPS FOR WILD CAUGHT SNAILS: m 27.1 MARGIZA DAM in 27.2 MARIDZANI DAM in 27.3 KISIAN STREAM (POOL 4) in 2 1 A KISIAN STREAM (POOL 1) u i 27.5 MIGOSI u i 27.6 P A P O N D I T I m 27.7 A S E M B O B A Y in 27.8 SHAMBA in 27.9 DUNGA BEACH i n 27.10 KINYUI 9 P f l O E : LIST OF TABLES 13 T A B L E 1 RECENT CLASSIFICATION OF THE GENUS Bulinus lb 2 D E T A I L S O F T H E FIVE N O M I N A L Bulinus africanus GROUP SPECIES IN KENYA 11 3 D E T A I L S O F T H E Bulinus africanus G R O U P SA M P L E S 4 S U MM AR Y OF VARIABLES USED IN THE PI AND P2 ANALYSES si 5 ENZYME ASSAY SOLUTIONS 5S 6 DETAILS OF THE SAMPLES ANALYSED BYC e l l u l o s e a c e t a t e electrophoresi b O 7 SUMMARY OF SAMPLE SIZE FOR EACH ANALYSIS 1 0 8 PI - NORMALISED EIGENVECTOR ELEMENTS ON THE FIRST THREE AXES FROM THE PRINCIPAL COMPONENT ANALYSIS OF 228 OTUS A N D 20 VARIABLES 1 9 PI - NORMALISED EIGENVECTOR ELEMENTS ON THE FIRST THREE AXES FROM THE PRINCIPAL COMPONENT ANALYSIS OF 228 OTUS A N D 20 VARIABLES, WITH ISOMETRIC SIZE-EFFECT REMOVED.
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    Chen et al. BMC Microbiology (2021) 21:200 https://doi.org/10.1186/s12866-021-02259-2 RESEARCH Open Access Composition and diversity of gut microbiota in Pomacea canaliculata in sexes and between developmental stages Lian Chen1, Shuxian Li2, Qi Xiao2, Ying Lin2, Xuexia Li1, Yanfu Qu2, Guogan Wu3* and Hong Li2* Abstract Background: The apple snail, Pomacea canaliculata, is one of the world’s 100 worst invasive alien species and vector of some pathogens relevant to human health. Methods: On account of the importance of gut microbiota to the host animals, we compared the communities of the intestinal microbiota from P. canaliculata collected at different developmental stages (juvenile and adult) and different sexes by using high-throughput sequencing. Results: The core bacteria phyla of P. canaliculata gut microbiota included Tenericutes (at an average relative abundance of 45.7 %), Firmicutes (27.85 %), Proteobacteria (11.86 %), Actinobacteria (4.45 %), and Cyanobacteria (3.61 %). The female group possessed the highest richness values, whereas the male group possessed the lowest bacterial richness and diversity compared with the female and juvenile group. Both the developmental stages and sexes had important effects on the composition of the intestinal microbiota of P. canaliculata. By LEfSe analysis, microbes from the phyla Proteobacteria and Actinobacteria were enriched in the female group, phylum Bacteroidetes was enriched in the male group, family Mycoplasmataceae and genus Leuconostoc were enriched in the juvenile group. PICRUSt analysis predicted twenty-four metabolic functions in all samples, including general function prediction, amino acid transport and metabolism, transcription, replication, recombination and repair, carbohydrate transport and metabolism, etc.
  • Studies on the Morphology and Compatibility Between Schistosoma Hæmatobium and the Bulinus Sp

    Studies on the Morphology and Compatibility Between Schistosoma Hæmatobium and the Bulinus Sp

    African Journal of Biotechnology Vol. 4 (9), pp. 1010-1016, September 2005 Available online at http://www.academicjournals.org/AJB ISSN 1684–5315 © 2005 Academic Journals Full Length Research Paper Studies on the morphology and compatibility between Schistosoma hæmatobium and the Bulinus sp. complex (gastropoda: planorbidae) in Cameroon Mimpfoundi Remy* and Ndassa Arouna General Biology Laboratory Faculty of Science, P.O Box 812 Yaoundé I Cameroon. Accepted March, 2005 A description is given of the morphological variation of the shell, the radula features and the copulatory organ of Bulinus sp. (2n=36) from four populations in the western Cameroon crater lakes. To assess the role of diploid snails belonging to the Bulinus natalensis/tropicus complex in the transmission of urinary schistosomiasis in Cameroon, the relation between Bulinus sp. (from four Cameroon crater lakes) and Schistosoma haematobium (from three transmission foci) were studied. Bulinus sp. in the present study refers to the diploid snail (2n=36) tentatively identified as Bulinus natalensis or as Bulinus tropicus in the Cameroon crater lakes. The percentage infection of snails challenged ranged from 03.33 to 06.00% for Nchout Monoun population and from 01.85 to 04.76% for Monoun Ngouondam population. No progeny from Petponoun-East and Petponoun-West were experimentally successfully infected with S. haematobium. All the 351 snails dissected were euphallic. Previous malacological surveys revealed the absence of Bulinus sp. naturally infected with human schistosomes. These results suggested that Bulinus sp. was not susceptible to infection with S. haematobium in the Cameroon Western highland crater lakes. These observations justify the absence of transmission foci (for urinary schistosomiasis) in this area.
  • THE STATUS and DISTRIBUTION of Freshwater Biodiversity in Madagascar and the Indian Ocean Islands Hotspot

    THE STATUS and DISTRIBUTION of Freshwater Biodiversity in Madagascar and the Indian Ocean Islands Hotspot

    THE THE STATUs aNd dISTRIBUtION OF STAT U Freshwater biodIversIty in MadagasCar s a N aNd the INdIaN OCeaN IslaNds hOtspOt d d I STR Edited by Laura Máiz-Tomé, Catherine Sayer and William Darwall IUCN Freshwater Biodiversity Unit, Global Species Programme IBU t ION OF F OF ION RESHWATER N ds a BIO I N d I ar ar VERS d C N I TY IN IN sla Madagas I N C ar a ar N ea d the I the d d the I the d C N N d Madagas a O I a N O C ea N I sla N IUCN h ds Rue Mauverney 28 CH-1196 Gland O Switzerland tsp Tel: + 41 22 999 0000 Fax: + 41 22 999 0015 O www.iucn.org/redlist t the IUCN red list of threatened speciestM www.iucnredlist.org THE STATUS AND DISTRIBUTION OF freshwater biodiversity in Madagascar and the Indian Ocean islands hotspot Edited by Laura Máiz-Tomé, Catherine Sayer and William Darwall IUCN Freshwater Biodiversity Unit, Global Species Programme The designation of geographical entities in this book, and the presentation of the material, do not imply the expression of any opinion whatsoever on the part of IUCN concerning the legal status of any country, territory, or area, or of its authorities, or concerning the delimitation of its frontiers or boundaries. The views expressed in this publication do not necessarily reflect those of IUCN, or other participating organisations. This publication has been made possible by funding from The Critical Ecosystem Partnership Fund. Published by: IUCN Cambridge, UK in collaboration with IUCN Gland, Switzerland Copyright: © 2018 IUCN, International Union for Conservation of Nature and Natural Resources Reproduction of this publication for educational or other non-commercial purposes is authorised without prior written permission from the copyright holder provided the source is fully acknowledged.