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BOOPHILUS MICROPLUS BABESIA THE SOUTPANSBERG REGION, NORTHERN PROVINCE, SOUTH AFRICA

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BOOPHILUS MICROPLUS BABESIA THE SOUTPANSBERG REGION, NORTHERN PROVINCE, SOUTH AFRICA
University of Pretoria etd – Tonnesen, M (2005)
DISTRIBUTION OF BOOPHILUS MICROPLUS AND
BOOPHILUS DECOLORATUS AND ASSOCIATED
OCCURRENCE OF BABESIA SPECIES IN CATTLE IN
THE SOUTPANSBERG REGION, NORTHERN
PROVINCE, SOUTH AFRICA
by
MIRJAM HAUKE TØNNESEN
Submitted in fulfilment of the requirements for the degree of
MAGISTER SCIENTIAE (Veterinary Sciences)
in the
Department of Veterinary Tropical Diseases
Faculty of Veterinary Science
University of Pretoria
Pretoria
2002
University of Pretoria etd – Tonnesen, M (2005)
Declaration
Apart from the assistance received that has been reported in the
Acknowledgements and in the appropriate places in the text,
this Dissertation represents the original work of the author.
No part of the Dissertation has been presented for
any other degree at any other University.
CANDIDATE
DATE
i
University of Pretoria etd – Tonnesen, M (2005)
SUMMARY
DISTRIBUTION
OF
BOOPHILUS
MICROPLUS
AND
BOOPHILUS
DECOLORATUS AND ASSOCIATED OCCURRENCE OF BABESIA SPECIES IN
CATTLE IN THE SOUTPANSBERG REGION, NORTHERN PROVINCE, SOUTH
AFRICA
by
Mirjam Hauke Tønnesen
Supervisor:
Prof. B. L. Penzhorn
Co-supervisor:
Dr. N. R. Bryson
Bovine babesiosis occurs worldwide and is one of the most costly tick-borne cattle
diseases in the tropics. The Soutpansberg region of the Northern Province in South Africa
is endemic for Babesia bigemina, but Babesia bovis was only reported from this area in
the 1980s when some farmers experienced heavy losses due to Asiatic redwater.
The main objectives of the study were to confirm the presence of the tick vector
Boophilus microplus in the Soutpansberg region where it had not been reported
previously, and to determine the seroprevalence of Babesia bovis and Babesia bigemina
in cattle in these areas. Other objectives were to assess the relative numbers of Boophilus
microplus in relation to Boophilus decoloratus and to determine a possible displacement
of Boophilus decoloratus by Boophilus microplus. It was also the intention to map the
potential distribution of the Boophilus ticks in the area and to more accurately predict the
further spread of Boophilus microplus.
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University of Pretoria etd – Tonnesen, M (2005)
Tick collections and serological surveys were carried out during 1999 and 2000 on cattle
at 30 communal dip tanks and on 5 commercial farms in the Soutpansberg, Dzanani,
Mutale, Thohoyandou and Vuwani Districts. Of the 25,042 Boophilus ticks collected,
93.9 % were Boophilus microplus and 6.1 % were Boophilus decoloratus. At 8 of the dip
tanks/farms both Boophilus species were found, and the displacement of Boophilus
decoloratus by Boophilus microplus was monitored at 4 of these sites. There was a
distinct displacement of Boophilus decoloratus at those dip tanks/farms where repeated
tick collection was possible.
Cattle at the communal dip tanks carried larger Boophilus tick numbers than cattle on the
commercial farms. Boophilus microplus was the most common Boophilus tick collected
at the dip tanks, and during the survey it also became the Boophilus tick most commonly
found on the commercial farms.
CLIMEX was used to map the potential distribution of Boophilus microplus and
Boophilus decoloratus in the survey area during years with average as well as double
average rainfall. Ecoclimatic Indices were computed for each sampling location, using 30
years of climatic information. The displacement patterns of Boophilus species were also
discussed.
Blood samples (n = 2201) were collected for Indirect Fluorescent Antibody (IFA) testing.
Serological evidence of Babesia bovis was detected in 97 % of the communal dip tank
herds and in 100 % of the commercial farm herds. The overall seroprevalence of Babesia
bovis in the dip tank herds during 1999 and 2000 was 63 %. The seroprevalence of
Babesia bovis in the commercial herds increased significantly from 19 % in 1999 to
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University of Pretoria etd – Tonnesen, M (2005)
57.5 % in 2000. There was a slight increase in endemic stability in comparable herds
from 1999 to 2000. The increase in seroprevalence and endemic stability probably came
as a result of the influx of Boophilus microplus into the survey area. There was a
significant correlation between the presence of Boophilus microplus in the survey area
and the increasing seroprevalence of Babesia bovis, which confirms that Boophilus
microplus is the main and probably the only vector of Babesia bovis in South Africa.
Serological evidence of Babesia bigemina was detected in 100 % of communal dip tank
and commercial farm herds. The overall seroprevalence of Babesia bigemina in the dip
tank herds decreased significantly from 56.1 % in 1999 to 49.3 % in 2000. There was a
marked decrease in endemic stability for Babesia bigemina in comparable dip tank herds
from 1999 to 2000. The decrease in seroprevalence and endemic stability to Babesia
bigemina in these herds was probably due to the substantial increase of Boophilus
microplus in the survey area. This may indicate that Babesia bigemina was transmitted
less effectively by Boophilus microplus than by Boophilus decoloratus.
The seroprevalence of Babesia bovis was significantly higher than that of Babesia
bigemina at those dip tanks/farms where only Boophilus microplus was present during
1999 and 2000. This may be explained by the possibility that Boophilus microplus
transmits Babesia bigemina less effectively than it transmits Babesia bovis.
This survey raises several questions on the ability of the African strain of Boophilus
microplus to transmit African Babesia strains. There are indications that the African
Boophilus microplus is different to the Australian Boophilus microplus. More research
needs to be done to investigate how the Babesia species are transmitted in Africa.
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University of Pretoria etd – Tonnesen, M (2005)
SAMEVATTING
VERSPREIDING
VAN
BOOPHILUS
MICROPLUS
EN
BOOPHILUS
DECOLORATUS EN DIE GEASSOSIEERDE VOORKOMS VAN BABESIA SPESIES
IN BEESTE IN DIE SOUTPANSBERGSTREEK, NOORDELIKE PROVINSIE, SUIDAFRIKA
deur
Mirjam Hauke Tønnesen
Promotor:
Prof B L Penzhorn
Mede-promotor:
Dr N R Bryson
Babesiose van beeste kom wêreldwyd voor en van groot ekonomiese belang in tropiese
streke. Babesia bigemina kom endemies voor in die Soutpansbergstreek van die
Noordelike Provinsie van Suid-Afrika, maar Babesia bovis is eers gedurende die 1980s
aangeteken, toe sommige boere swaar verliese gely het.
Die hoofdoel van hierdie ondersoek was om die teenwoordigheid van die oordraerbosluis
Boophilus microplus in die Soutpansbergstreek te bevestig en om die seroprevalensie van
Babesia bovis en Babesia bigemina in beeste in die streek te bepaal. Verder is gepoog om
die aantal Boophilus microplus in verhouding tot Boophilus decoloratus vas te stel en om
die moontlike verplasing van Boophilus decoloratus deur Boophilus microplus te
dokumenteer. Laastens is gepoog om die potensiële verspreiding van Boophilus spesies te
karteer sodat die verdere verspreiding Boophilus microplus meer noukeurig voorspel kan
word.
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University of Pretoria etd – Tonnesen, M (2005)
Bosluise en serummonsters is tydens 1999 en 2000 van beeste by 30 gemeenskaplike
dipbakke en op 5 plase in die Soutpansberg-, Dzanani-, Mutale-, Thohoyandou- en
Vuwanidistrik versamel. Van die 23,042 Boophilus bosluise wat versamel is, was 93.9 %
Boophilus microplus en 6.1 % Boophilus decoloratus. Albei Boophilus spesies het by 8
dipbakke/plase voorgekom en die verplasing van Boophilus decoloratus deur Boophilus
microplus is by 4 van hulle gevolg. Verplasing van Boophilus decoloratus was ‘n
duidelike neiging by dié dipbakke/plase waar opeenvolgende versameling moontlik was.
Bosluisladings van beeste by die gemeenskaplike dipbakke was hoër as dié op plase.
Boophilus microplus was die algemeenste bosluis wat by die dipbakke versamel is, en
tydens die ondersoek het dit ook die algemeenste Boophilus spesie op die plase geword.
CLIMEX is gebruik om die potensiële verspreiding van Boophilus microplus en
Boophilus decoloratus in die studiegebied te voorspel, in gemiddelde reënjare asook
wanneer die reënval sou verdubbel. Ekoklimatiese indekse is vir elke monsterpunt
bereken, aan die hand van klimaatgegewens van die afgelope 30 jaar. Die patroon van
verplasing van die onderskeie Boophilus spesies is bespreek.
Bloedmonsters (n = 2201) is versamel vir Indirect Fluorescent Antibody (IFA)-toetse.
Serologiese getuienis van die voorkoms van Babesia bovis is by 97 % van die
gemeenskaplike dipbakke en op 100 % van die plase gevind. Tydens 1999 en 2002 was
die algehele seroprevalensie van Babesia bovis in kuddes by gemeenskaplike dipbakke
63 %. Die seroprevalensie van Babesia bovis op plase het betekenisvol gestyg van 19 %
in 1999 tot 57.5 % in 2000. Daar was ‘n effense toename in endemiese stabiliteit in
vergelykbare kuddes van 1999 tot 2000. Die toename in seroprevalensie en endemiese
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University of Pretoria etd – Tonnesen, M (2005)
stabiliteit hou waarskynlik verband met ‘n instroming van Boophilus microplus in die
studiegebied. Daar was ‘n beteknisvolle korrelasie tussen die teenwoordigheid van
Boophilus microplus en die toenemende seroprevalensie van Babesia bovis, wat bevestig
dat Boophilus microplus die hoof en waarskynlik die enigste oordraer van Babesia bovis
in Suid-Afrika is.
By die dipbakke / plase waar slegs Boophilus microplus in 1999 en 2000 voorgekom het,
was die seroprevalensie van Babesia bovis betekenisvol hoër as dié van Babesia
bigemina. Die verduideliking mag daarin lê dat Babesia bigemina minder doeltreffend as
Babesia bovis deur Boophilus microplus oorgedra word.
Serologiese bewys van Babesia bigemina is by al die kuddes by dipbakke en op plase
gevind. Die seroprevalensie van Babesia bigemina onder kuddes by dipbakke het
betekenisvol gedaal van 56.1 % in 1999 tot 49.3 % in 2000. Daar was ‘n aanmerklike
afname in endemiese stabiliteit vir Babesia bigemina in ooreenstemmende dipbakkuddes
tussen 1999 en 2000. Die afname in seroprevalensie en endemiese stabiliteit van Babesia
bigemina mag verband hou met die oorwig Boophilus microplus in die studiegebied. Dit
mag daarop dui dat Babesia bigemina nie so doeltreffend deur Boophilus microplus as
deur Boophilus decoloratus oorgedra word nie.
Hierdie sudie laat verskeie vrae ontstaan oor die vermoë van die Afrika-stamme van
Boophilus microplus om Afrika-stamme van Babesia oor te dra. Daar is aanduidings dat
Boophilus microplus in Afrika verskil van Boophilus microplus in Australië; meer
navorsing word geverg om vas te stel hoe Babesia bovis en Babesia bigemina in Afrika
oorgedra word.
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University of Pretoria etd – Tonnesen, M (2005)
TABLE OF CONTENTS
TOPIC
PAGE
DECLARATION…………………………………………………………………………….i
SUMMARY…………………………………………………………………………….…....ii
SAMEVATTING………………………………………………………………….…………v
TABLE OF CONTENTS………………………………………………………………….viii
LIST OF TABLES……………………………………………………………….……………………….xvi
LIST OF FIGURES………………………………………………………………….…….xxi
LIST OF PERSONAL COMMUNICATIONS…………………………………………xxiii
ACKNOWLEDGEMENTS…………………………………………………………….…xxv
CHAPTER 1. INTRODUCTION
1. 1 Importance of bovine babesiosis worldwide……………………………….…1
1. 1. 1 The Babesia parasites………………………………………………..1
1. 2 The historical importance of bovine babesiosis in Africa……………………2
1. 3 Importance of bovine babesiosis in South Africa…………………………….3
1. 3. 1 General………………………………………………………….…….3
1. 3. 2 Importance of bovine babesiosis in the study area………………...3
1. 4 The main objectives of the study……………………………………………….5
CHAPTER 2. LITERATURE REVIEW
2. 1 The genus Babesia………………………………………………………………7
2. 1. 1 Comparative morphology and strain differences:…………………7
2. 1. 2 Diagnosis of redwater…………………………………………….….8
2. 1. 3 Geographical distribution in South Africa…………………………9
2. 1. 4 Transmission by the vectors……………………………………….11
2. 1. 5 Clinical signs of the diseases…..…………………………………...12
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2. 1. 6 Pathogenesis of bovine babesiosis……………………………..…..13
2. 1. 7 Pathology………………………………………...………………….13
2. 1. 8 Immunity………………………………………………………...….14
•
General immunity.……………………………………….……..14
•
Age-dependent immunity………….…………………….……..15
•
Breed-dependent immunity……………………………………16
2. 1. 9 Endemic stability to redwater……………………………………..18
2. 2 The tick vectors of bovine babesiosis in southern Africa………….…….…..20
2. 2. 1 Boophilus species on domestic and wild animals
in southern Africa………….…………………………..…………...20
2. 2. 2 Characteristics of the genus Boophilus……………………………21
2. 2. 3 Comparative morphology…..……………………………….……..21
2. 2. 4 Geographical distribution and seasonal incidence of Boophilus
decoloratus and Boophilus microplus in southern Africa…..…….22
2. 2. 4. 1 Distribution of Boophilus decoloratus in
southern Africa ………………………………………….23
2. 2. 4. 2 Distribution of Boophilus microplus in southern
Africa …………………………………………………….26
2. 2. 5 Interbreeding and competition between Boophilus species……..29
2. 2. 6 Infection rates of Babesia species in Boophilus species…………..32
2. 2. 6. 1 Observed Babesia bigemina and Babesia bovis
infections in ticks……….………………………………..32
2. 2. 6. 2 Infectivity of ticks to cattle...…………………………….33
2. 2. 7 Environmental factors affecting the Babesia parasites in
the tick………………………………………………………………34
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University of Pretoria etd – Tonnesen, M (2005)
2. 2. 8 Inoculation rate………….………………………………….……...34
2. 2. 9 Breed resistance against Boophilus species…………………....…35
2. 2. 10 Other factors affecting host resistance against Boophilus
species……………………………………………………………...36
2. 3 The role of models in tick control………………………………………….…37
2. 3. 1 CLIMEX…….………………………………………………….…...37
2. 3. 2 Earlier predictions………………………………….……………….38
CHAPTER 3. MATERIALS AND METHODS
3. 1. Survey areas……………………………………………………………..…….39
3. 1. 1 The communal farming areas………...………………….………..40
3. 1. 1. 1 Location of the different communal dip tanks……..…...41
3. 1. 1. 2 Vegetation types and climatic conditions at the
dip tanks………………………………………………….45
3. 1. 2 The commercial farming areas………………..…...………………48
3. 1. 2. 1 Detailed description of the five commercial farms…..…49
3. 1. 2. 2 Vegetation types and climatic conditions on
the commercial farms………………………………..…..53
3. 2 Experimental design……………………………………………..…………….55
3. 2. 1 Sample selection……..……………………………………………..55
3. 2. 2 Sample population in the study area……………………….……..56
3. 2. 3 Blood collection……………………………………………………..57
3. 2. 4 Tick collection………………………………………………………58
3. 3 Serological procedures………………………….………………………….….59
3. 3. 1 Detection of antibodies…………………………………….……….59
3. 4 CLIMEX mapping……………………………………………………………..60
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University of Pretoria etd – Tonnesen, M (2005)
3. 4. 1 The CLIMEX maps…………………………………………………60
3. 4. 2 Climatic information…….………………………………………….60
3. 5 Statistical analysis……………………………………………………………...60
3. 5. 1 Computing of probabilities.………………………………………..60
CHAPTER 4. RESULTS
4. 1 Serological findings…………………………………………………………….62
4. 1. 1 Seroprevalence of antibodies to Babesia bovis and Babesia
bigemina collected from cattle at the communal dip tanks
during 1999 and 2000………………………………………………62
4. 1. 1. 1. Seroprevalence of antibodies to Babesia bovis and
Babesia bigemina collected from cattle bled at
dip tanks situated in the Sour Lowveld Bushveld
veld type during 1999……………………………………69
4. 1. 2 Seroprevalence of antibodies to Babesia bovis and Babesia
bigemina collected from cattle on the commercial farms
during 1999 and 2000………….…………………………………...76
4. 1. 3 A comparison of the seroprevalence of antibodies to Babesia
bovis and Babesia bigemina in cattle bled at communal dip
tanks and commercial farms during 1999 and 2000………………..80
4. 2 Endemic stability to Babesia bovis and Babesia bigemina…………………...82
4. 2. 1 Endemic stability to Babesia bovis and Babesia bigemina
in cattle at the communal dip tanks during 1999 and 2000……...82
4. 2. 2 Endemic stability to Babesia bovis and Babesia bigemina
recorded on the commercial farms during 1999 and 2000….…...84
4. 3 Tick collection results from the survey area during 1999 and 2000………...86
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University of Pretoria etd – Tonnesen, M (2005)
4. 3. 1 Tick collection results from the communal dip tanks during
1999 and 2000……………………………………………………….87
4. 3. 2 Tick collection results from the commercial farms during
1999 and 2000……………………………………………………….89
4. 4 Displacement of Boophilus decoloratus by Boophilus microplus in the
survey area……………………………………………………………………...91
4. 4. 1 Tick collection results recorded during the displacement
process……………………………………………………….……....91
4. 4. 2 Ecoclimatic Indices for Boophilus microplus and Boophilus
decoloratus recorded at the communal dip tanks and
commercial farms……………………………………….…….….…92
4. 5 Comparison of the Boophilus tick numbers and the serology results
obtained during 1999 and 2000………………………………………..….…...93
CHAPTER 5. DISCUSSION
5. 1 Serological findings………………………………………………………..…..97
5. 1. 1 Interpretation of the IFAT……….………………………………...97
5. 1. 2 Serological cross-reactions…….…………………………………...98
5. 1. 3 Serological findings from cattle sampled at communal dip
tanks during1999 and 2000………………………………………..99
5. 1. 4 Serological findings from cattle sampled on the commercial
farms during 1999 and 2000………………………………….…...103
5. 1. 5 Statistical significance of the serological results from the
communal dip tanks and the commercial farms………………...107
5. 2 Endemic stability to Babesia bovis and Babesia bigemina…………….……108
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5. 2. 1 Endemic stability to Babesia bovis and Babesia bigemina
found in the cattle sampled at the dip tanks during
1999 and 2000……………………………………………………...109
5. 2. 2 Endemic stability to Babesia bovis and Babesia bigemina
found in the cattle sampled on the commercial farms during
1999 and 2000……………………………………………………...111
5. 2. 3 Endemic stability to Babesia bovis and Babesia bigemina
at the dip tanks compared with endemic stability
on the commercial farms……………………………………..….. 112
5. 2. 4 Correlation between the endemic stability to Babesia bovis
and Babesia bigemina at dip tanks/farms and the presence of
specific Boophilus species…………….…..……………………….113
5. 3 Tick collections in the survey area…………………………………….…….114
5. 3. 1 General discussion of the tick results……………………………..114
5. 3. 2 Reasons for the variation in tick numbers in the study area……115
5. 3. 3 Tick collection from cattle at the dip tanks…….………………....117
5. 3. 4 Tick collections from cattle on the commercial farms…………...118
5. 3. 5 Boophilus tick collections from the communal dip tanks
compared with those from the commercial farms………....….…120
5. 4 Displacement of Boophilus decoloratus by Boophilus microplus in
the survey area……………………………………………………..…………121
5. 4. 1 Introduction…………………………………………………...…....121
5. 4. 2 Tick findings in the survey area showing displacement…..……. 122
5. 4. 3 The use of the CLIMEX Ecoclimatic Index (EI) and the
CLIMEX maps…………………………………………………….124
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5. 5 Possible association between the Babesia seroprevalence and the
presence of Boophilus tick species collected at the communal dip
tanks and the commercial farms during 1999 and 2000…………………....133
5. 5. 1 Introduction…………………………....…………………………...133
5. 5. 2 Possible association between the Boophilus tick species
on the cattle and the mean Babesia bovis seroprevalence………133
5. 5. 2. 1 Factors affecting the Babesia bovis
seroprevalence during the survey………..……………134
5. 5. 3 Possible association between the Boophilus tick species on
cattle and the mean Babesia bigemina seroprevalence…………136
5. 5. 4 Possible association between the seroprevalence of
Babesia bovis and Babesia bigemina and the presence of
Boophilus ticks at the dip tanks/farms…………………………..138
5. 5. 5 Possible association between the relative abundance of
Boophilus ticks at the dip tanks/farms compared with the
seroprevalence to Babesia bovis and Babesia bigemina.………...139
5. 5. 6 Changes in seroprevalence of Babesia bovis and Babesia
bigemina in the cattle at single dip tanks/farms where
displacement of Boophilus decoloratus by Boophilus
microplus was monitored…………………………………….……140
5. 5. 7 The ability of the different Boophilus ticks to transmit Babesia
species………………………………………………………………142
CHAPER 6. CONCLUSIONS AND RECOMMENDATIONS
6. 1. 1 Conclusions on the displacement of Boophilus decoloratus
by Boophilus microplus…………………………………………...144
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6. 1. 2 The association between the EI, tick numbers and Babesia
serology recorded at each dip tank/farm………………………...147
6. 1. 3 Recommendations……………………………………….……..…..149
CAPTER 7. REFERENCES………………………………………………………….…..152
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LIST OF TABLES
Table
Table 4. 1
Page
Seroprevalence of antibodies to Babesia bovis and Babesia
bigemina in both age groups of cattle bled at dip tanks during 1999…...62
Table 4. 2
Seroprevalence of antibodies to Babesia bovis and Babesia
bigemina in cattle older than 18 months bled at dip tanks
during 1999…………………………………………………………………63
Table 4. 3
Seroprevalence of antibodies to Babesia bovis and Babesia bigemina
in cattle aged 4-14 months bled at dip tanks during 1999……………….64
Table 4. 4
Seroprevalence of antibodies to Babesia bovis and Babesia
bigemina in both age groups of cattle bled at dip tanks during 2000.…..65
Table 4. 5
Seroprevalence of antibodies to Babesia bovis and Babesia bigemina
in cattle older than 18 months bled at dip tanks during 2000…………..66
Table 4. 6
Seroprevalence of antibodies to Babesia bovis and Babesia bigemina
in cattle aged 4-14 months bled at dip tanks during 2000……………….67
Table 4. 7
Chi–square test of the differences in the seroprevalence of
Babesia bovis and Babesia bigemina from cattle bled at the
communal dip tanks during 1999 and 2000, compared by age….….…..68
Table 4. 8
Chi–square test of the differences in the seroprevalence of
Babesia bovis and Babesia bigemina from cattle bled at the
communal dip tanks during 1999 and 2000, compared by year…………68
Table 4. 9
Seroprevalence of antibodies to Babesia bovis and Babesia
bigemina in both age groups of cattle bled at dip tanks situated
in the Sour Lowveld Bushveld veld type during 1999 …………………...69
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University of Pretoria etd – Tonnesen, M (2005)
Table 4. 10
Seroprevalence of antibodies to Babesia bovis and Babesia
bigemina in cattle older than 18 months bled at dip tanks
situated in the Sour Lowveld Bushveld veld type during 1999………….70
Table 4. 11
Seroprevalence of antibodies to Babesia bovis and Babesia
bigemina in cattle aged 4-14 months bled at dip tanks situated
in the Sour Lowveld Bushveld veld type during 1999……………………71
Table 4. 12
Seroprevalence of antibodies to Babesia bovis and Babesia
bigemina in both age groups of cattle bled at dip tanks situated
in the Sour Lowveld Bushveld veld type during 2000………………...…72
Table 4. 13
Seroprevalence of antibodies to Babesia bovis and Babesia
bigemina in cattle older than 18 months bled at dip tanks
situated in the Sour Lowveld Bushveld veld type during 2000………….73
Table 4. 14
Seroprevalence of Babesia bovis and Babesia bigemina in
cattle aged 4-14 months bled at dip tanks situated in the Sour
Lowveld Bushveld veld type during 2000………………………………...74
Table 4. 15
Chi–square test of the differences in the seroprevalence of Babesia
bovis and Babesia bigemina from cattle bled at the communal dip
tanks situated in the Sour Lowveld Bushveld veld type during 1999
and 2000, compared by age.……………………………………………….75
Table 4. 16
Chi–square test of the differences in the seroprevalence of Babesia
bovis and Babesia bigemina from cattle bled at the communal dip
tanks situated in the Sour Lowveld Bushveld veld type during 1999
and 2000, compared by year.. …………………………………………….75
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Table 4. 17
Seroprevalence of antibodies to Babesia bovis and Babesia
bigemina in both age groups of cattle bled on the commercial
farms during 1999…………………………………………………………..76
Table 4. 18
Seroprevalence of antibodies to Babesia bovis and Babesia
bigemina in cattle older than 18 months bled on commercial
farms during 1999………………………………………………………….76
Table 4. 19
Seroprevalence of antibodies to Babesia bovis and Babesia
bigemina in cattle aged 4-14 months bled on commercial farms
during 1999…….……………………………………………………………77
Table 4. 20
Seroprevalence of antibodies to Babesia bovis and Babesia
bigemina in both age groups of cattle bled on commercial
farms during 2000………….……………………………………………….77
Table 4. 21
Seroprevalence of antibodies to Babesia bovis and Babesia
bigemina in cattle older than 18 months bled on commercial
farms during 2000…………………………………………………………..78
Table 4. 22
Seroprevalence of antibodies to Babesia bovis and Babesia
bigemina in cattle aged 4-14 months bled on commercial
farms during 2000………………………………………………..…………78
Table 4. 23
Chi–square test of the differences in the seroprevalence of
antibodies to Babesia bovis and Babesia bigemina from cattle bled
at commercial farms during 1999 and 2000, compared by age………….79
Table 4. 24
Chi–square test of the differences in the seroprevalence of
antibodies to Babesia bovis and Babesia bigemina from cattle bled
at commercial farms during 1999 and 2000, compared by year…………79
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University of Pretoria etd – Tonnesen, M (2005)
Table 4. 25
Chi-square test of the differences in the seroprevalence of
antibodies to Babesia bovis and Babesia bigemina in cattle bled at
the communal dip tanks and the commercial farms during
1999 and 2000……………………………………………………………….80
Table 4. 26
Chi-square test of the differences in the seroprevalence of
antibodies to Babesia bovis and Babesia bigemina in all cattle bled
at the communal dip tanks and the commercial farms during 1999
and 2000, compared by year….…………………………………………….80
Table 4. 27
Boophilus ticks collected from cattle at dip tanks during 1999………….87
Table 4. 28
Boophilus ticks collected from cattle at dip tanks during 2000………….88
Table 4. 29
Boophilus ticks collected from cattle on commercial farms
during 1999..……………………………………………………….………...89
Table 4. 30
Boophilus ticks collected from cattle on commercial farms
during 2000 and 2001……………………………………………..………..90
Table 4. 31
Tick collections obtained by repeatedly sampling farms and/or
dip tanks where Boophilus decoloratus and Boophilus microplus
co-existed during the survey ………………………………………………91
Table 4. 32
Ecoclimatic Indices for B. microplus and B. decoloratus………………...92
Table 4. 33
Mean seroprevalence of Babesia bovis and Babesia bigemina
from those dip tanks/farms where only Boophilus decoloratus
was recorded in 1999……………………………………………………….93
Table 4. 34
Mean seroprevalence of Babesia bovis and Babesia bigemina
from those dip tank/farms where Boophilus decoloratus and
Boophilus microplus co-existed in 1999……………………………………93
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Table 4. 35
Mean seroprevalence of Babesia bovis and Babesia bigemina
from those dip tank/farms where only Boophilus microplus was
recorded in 1999……………………………………………………………94
Table 4. 36
Mean seroprevalence of Babesia bovis and Babesia bigemina
from those dip tanks/farms where Boophilus decoloratus and
Boophilus microplus co-existed in 2000……………………………………94
Table 4. 37
Mean seroprevalence of Babesia bovis and Babesia bigemina
from those dip tanks/farms where only Boophilus microplus
was recorded in 2000……………………………………………………….95
Table 4. 38
Summary of seroprevalence of Babesia bigemina and Babesia
bovis related to vector occurrence at all dip tanks/farms
sampled during 1999……………………………………………………..…96
Table 4. 39
Summary of seroprevalence of Babesia bigemina and Babesia
bovis related to vector occurrence at all dip tanks/farms
sampled during 2000……………………………………………..…………96
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LIST OF FIGURES
Figure
Fig. 1. 1
Page
Confirmed cases of bovine babesiosis in the study area in
1997, 1998 and 1999…………………………………………………………5
Fig. 2. 1
Map showing the geographical distribution of Babesia bigemina and
Babesia bovis in South Africa …………………………………….……….10
Fig. 3. 1
Map of the Northern Province of South Africa showing
the survey area……………………………………………………………...39
Fig. 4. 1
Endemic stability to Babesia bovis recorded at the 11 dip tanks
in the survey during 1999………………………………………....………..82
Fig. 4. 2
Endemic stability to Babesia bovis recorded at the 19 dip tanks
in the survey during 2000…………………………………………………..82
Fig. 4. 3
Endemic stability to Babesia bigemina recorded at the 11 dip tanks
in the survey during 1999…………………………………………………..83
Fig. 4. 4
Endemic stability to Babesia bigemina recorded at the 19 dip tanks
in the survey during 2000………………………………………..…………83
Fig. 4. 5
Endemic stability to Babesia bovis recorded on the 5 commercial
farms in the survey during 1999………………………………....…………84
Fig. 4. 6
Endemic stability to Babesia bovis recorded on the 2 commercial
farms in the survey during 2000…………………………….….…………..84
Fig. 4. 7
Endemic stability to Babesia bigemina recorded on the
5 commercial farms in the survey during 1999……………………………85
Fig. 4. 8
Endemic stability to Babesia bigemina recorded on the
2 commercial farms in the survey during 2000…………………………..85
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Fig. 5. 1
CLIMEX Ecoclimatic Index map illustrating the predicted
distribution of Boophilus microplus in years with average rainfall……129
Fig. 5. 2
CLIMEX Ecoclimatic Index map illustrating the predicted
distribution of Boophilus microplus in years with double
average rainfall……………………………………………………………130
Fig. 5. 3
CLIMEX Ecoclimatic Index map illustrating the predicted
distribution of Boophilus decoloratus in years with average rainfall…..131
Fig. 5. 4
CLIMEX Ecoclimatic Index map illustrating the predicted
distribution of Boophilus decoloratus in years with double
average rainfall……………………………………………………………132
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LIST OF PERSONAL COMMUNICATIONS
AHRENS PETER. P.O.Box 190, Louis Trichardt 0920, South Africa.
Tel (015) 516 0806
BAKER JAMES A.F. 17 Nahoon Crescent, Beacon Bay 5241, East London, South Africa.
Tel (043) 748 6374
BACKX ANOEK. Parkstraat 47, 3581 PE Utrecht, The Netherlands.
E-mail [email protected]
DE WAAL THEO D. ARC Onderstepoort Veterinary Institute. Private Bag X5,
Onderstepoort 0110, South Africa. Tel (012) 529 9212 E-mail [email protected]
GOUS TERTIUS A. P.O.Box 2269, Dennesig 7601, South Africa. Tel (021) 887 0324
E-mail [email protected]
LOOCK PIETER J. Veterinary Laboratory, Louis Trichardt. Private Bag 2408, Louis
Trichardt 0920, South Africa. Tel (015) 516 4971
LYNEN GODLIEVE. P.O.Box 1068, Veterinary Investigation Centre (Ministry of Water
and Livestock Development). Arusha, Tanzania.
E-mail: [email protected]
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University of Pretoria etd – Tonnesen, M (2005)
MACDONALD ANGUS. P.O.Box 481, Louis Trichardt 0920, South Africa.
Tel (015) 516 4791
OLDREIVE FRANK. P.O.Box 40, Munnik 0703, South Africa. Tel (015) 253 4435
SPICKETT ARTHUR M. ARC Onderstepoort Veterinary Institute. Onderstepoort 0110,
South Africa. Tel (012) 529 9209 E-mail [email protected]
SUTHERST ROBERT W (BOB). CSIRO Entomology, Long Pocket Laboratories, 120
Meiers Rd, Indooroopilly, Queensland, Australia 4068 Tel 61 (0)7 3214 2800 Fax 61 (0)7
3214 2885 E-mail [email protected]
TSHISAMPHIRI MASIBIGIRI (AGGREY). Veterinary Laboratory, Sibasa. Private Bag
2224, Sibasa 0970, South Africa. Tel (015) 963 1031
WILSON STEPHEN. P.O.Box 73, Waterpoort 7975, South Africa. Tel (015) 575 1095
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AKNOWLEDGEMENTS
I express my sincere appreciation and thanks to the following people:
UNIVERSITY OF PRETORIA
Prof. Banie Penzhorn, Department of Veterinary Tropical Diseases, was the main
promoter for the project and never stopped believing that the project was feasible.
Dr Nigel Bryson, Department of Veterinary Tropical Diseases, was a co-promoter and
spent time and energy guiding me through the difficult passages of my work.
Dr Hein Stoltsz, Department of Veterinary Tropical Diseases, was a co-worker and
contributed his unique knowledge and input to the project.
Prof. Ivan Horak, Department of Veterinary Tropical Diseases, gave invaluable advice
on tick taxonomy and made me laugh when life was difficult. He is a real Mensch.
Prof. Roy Tustin, Department of Veterinary Tropical Diseases, proof-read the
manuscript.
Dr Jannie Crafford and Dr Jackie Pickard, Department of Veterinary Tropical
Diseases, helped by solving computer problems.
Prof. Bruce Gummow, Department of Production Animal Studies, Section of
Epidemiology, supplied help and advice on the epidemiological aspects of the project.
Mrs Rina Owen and Mr Solly Millard, Department of Statistics, showed great
patience in explaining the mysteries of statistics and delivering understandable
explanations of the results.
Prof. Koos Coetzer, Head of Department of Veterinary Tropical Diseases, gave general
help and support to the project and allowed me to use the laboratory facilities and
equipment of the Department.
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The staff of the Department of Veterinarian Tropical Diseases, Faculty of
Veterinary Science, was helpful in solving everyday problems.
The staff in the Library, Faculty of Veterinary Sciences, supplied information quickly
and with great skill.
ONDERSTEPOORT VETERINARY INSTITUTE
Dr Theo de Waal supplied information on the serological tests regarding their validity,
specificity and sensitivity. He never saw problems, only solutions.
Mrs Andrea Spickett of the Serology Laboratory at the OVI did the serological tests
and gave great service.
Mr Arthur Spickett helped me with advice and background information.
Dr Deon van der Merwe patiently sorted out the veld types and the CLIMEX maps for
me and gave the project an interesting angle.
Mrs Heloise Heyne confirmed the identity of difficult ticks.
THE VETERINARY LABORATORY IN SIBASA
Mr Tshisamphiri Masibigiri “Agrey”, Veterinary Technologist, was a co-worker on
the project and organised the day-to-day work at the dip tanks. His assistance with the
farmers was invaluable and his tireless help on the ground was essential in making the
project become a reality.
Dr Shumani Mulaudzi, State Veterinarian. His staff helped with the collection of the
ticks and blood samples and allowed me to use the laboratory facilities.
Mr Simon Bonyane, Animal Health Technician, contributed by organising of the
fieldwork and by keeping people happy with his great sense of humour.
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Mr Reckson Sihadi, laboratory auxiliary, helped with the lab work.
THE VETERINARY LABORATORY IN LOUIS TRICHARDT
Dr Pieter Loock, State Veterinarian, laid the groundwork for the project, contacted the
commercial farmers in the survey and organised specimen collection/ laboratory
facilities. He and his family were a great source of encouragement.
Mrs Monja Maree, Veterinary Technologist, organised the work on the commercial
farms and in the laboratory. Her warm personality and her enjoyment of the work were
important for the project.
Mr Samuel Ramalamula, laboratory auxiliary, assisted with the bleeding and the
laboratory work. His quiet sense of humour and competent handling of the cattle was
important for the team effort.
THE MAPS
Prof. Roland Schultze, University of Natal, Pietermaritzburg, let me use 30 years of
climatic information from the Northern Province and made the maps possible.
Dr Robert (Bob) Sutherst, CSIRO, Queensland, Australia, is thanked for many
reasons: his never-ending encouragement and belief in the project and his invaluable
advice on ticks, climatic information and the use of the CLIMEX computer programme.
He connected me with scientists all over the world who spent time and effort to answer
my impertinent questions. Most of all he is thanked for making me laugh when I wanted
to give up and go home.
Mr Rick Bottomley, CSIRO, Queensland, Australia, sorted out the climatic data and
messy dip tank co-ordinates with great patience and skill.
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Mr Robert A. Pullen and Mr Charles E. Sellick supplied me with maps of Venda
when the dip tanks seemed lost in space, and helped me to anchor them firmly to coordinates.
ACCOMMODATION
Ms Elsa Schrenk was the owner “The Lourie” Country Inn in Levubu. She made my
long stay comfortable by looking after me, supplying delicious food at odd hours and
providing perfect accommodation.
Mr and Mrs Angus MacDonald and their family opened their home to me and became
my friends.
FUNDING
Statens lånekasse for utdanning, Oslo, Norway, contributed 85,000 NKr (ca R 60, 000) to
the project.
National Research Foundation , South Africa, contributed R 10, 000.
Statens dyrehelsetilsyn, Oslo, Norway, contributed 5,000 NKr (ca R 3,800).
Den norske veterinærforening, Oslo, Norway, contributed 4,000 NKr (ca R 3,000).
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CHAPTER 1. INTRODUCTION
1. 1. Importance of bovine babesiosis worldwide.
Bovine babesiosis or redwater occurs worldwide, with the exception of a few countries
where it is too cold for the tick vectors to survive (Hoyte, 1976; Callow et al., 1976b;
McCosker, 1981). Babesia bigemina and Babesia bovis historically caused the most
widespread tick-borne diseases and continue to be among the greatest obstacles to the
development of the livestock industry in tropical and subtropical regions of the world.
They are still important causes of mortality in cattle (McCosker, 1981) and as many as
one billion cattle worldwide are thought to be exposed to redwater (Mahoney, 1976, as
cited by Smith and Kakoma, 1989).
1. 1. 1. The Babesia parasites. The Babesias are protozoan parasites belonging to the
phylum
Apicomplexa,
class
Sporozoasida,
order
Eucoccidiorida,
suborder
Piroplasmorina and family Babesiidae (Levine, 1971). The parasites are usually hostspecific (Callow and Dalgliesh, 1982). The four Babesia species responsible for
redwater in cattle are Babesia bovis (syn. Babesia argentina) (Riek, 1968; Hoyte, 1976;
Callow et al., 1976b; Potgieter, 1977), Babesia bigemina, Babesia divergens and
Babesia major, but the latter two species do not occur in South Africa. Babesia
bigemina and Babesia bovis, the two important species found in cattle in South Africa,
are transmitted by one-host ticks of the genus Boophilus. Boophilus decoloratus
transmits only Babesia bigemina, whilst Boophilus microplus transmits both Babesia
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University of Pretoria etd – Tonnesen, M (2005)
bigemina and Babesia bovis (Potgieter, 1977). Babesia bigemina can also be transmitted
by Rhipicephalus evertsi evertsi (Büscher, 1988).
1. 2. The historical importance of bovine babesiosis in Africa.
When Europeans first colonized southern Africa they introduced highly susceptible
cattle which soon suffered heavy losses due to redwater. Babesia bigemina, the cause of
African redwater, appeared to have been present in the indigenous cattle, but caused few
clinical problems (Lawrence and Norval, 1979). Fatal cases of the disease in the
indigenous cattle only occasionally occurred (Theiler, 1975) as they seemed to acquire
immunity as young calves (Norval et al., 1992a). In 1893 Smith and Kilborne first
demonstrated that Babesia bigemina was transmitted by a tick vector, Boophilus
annulatus, in the USA (Levine, 1971; Hoyte, 1976; Smith and Kakoma, 1989; Brown et
al., 1990). In 1898 Koch established that Boophilus decoloratus was the main vector of
Babesia bigemina in Africa (Neitz, 1941).
The European settlers in Africa soon realized that young cattle were less susceptible to
bovine babesiosis than adult cattle and that cattle from known redwater areas could
survive when moved to new redwater endemic areas. Cattle could also be moved to new
areas in winter, when tick worry was minimal (Lawrence and Norval, 1979). The blood
parasite first encountered in these areas was Babesia bigemina which was indigenous to
Africa. However, after the rinderpest epidemic in 1896, Boophilus microplus-infested
cattle carrying Babesia bovis were imported from southern Asia via Madagascar to the
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African continent (Theiler and Robinson, 1954; Callow, 1977; Lawrence and Norval,
1979). Babesia bovis, the cause of Asiatic redwater, then spread from the eastern
coastline of South Africa and Mozambique into the interior of these countries and into
Zimbabwe and Zambia. Its spread was dependent on the presence of the vector,
Boophilus microplus, which has since continued to spread into new areas of southern
Africa (Howell et al., 1978; Norval and Short, 1984).
1. 3. Importance of bovine babesiosis in South Africa.
1. 3. 1. General. Tick-borne diseases (TBD) are economically important in southern
Africa, and bovine babesiosis is one of the most prevalent and widespread in these
regions. De Vos (1979) stated that 85 % of the cattle population in South Africa was
potentially at risk to bovine babesiosis; in 1971 nearly 8000 cattle died in KwaZuluNatal alone (De Vos and Every, 1981). In 1981 it was estimated that the cost of
controlling TBD in South Africa could be as high as 70 million Rand (De Vos, 1981).
When dipping broke down in Zimbabwe due to civil war (1973 – 1980), nearly a million
cattle died of TBD. Many of the deaths were due to Babesia infections and in some areas
cattle mortality due to TBD was nearly 95 % (Norval, 1979).
1. 3. 2. Importance of bovine babesiosis in the study area. The farming systems in the
area, which is situated in the northern part of the Northern Province, are divided into
commercial and subsistence (small-scale) farming. Historically there has been a dipping
service for the subsistence farmers, subsidized by the state and provincial governments.
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Dipping is undertaken to control the ticks that transmit East Coast fever, African
redwater, Asiatic redwater, heartwater and anaplasmosis (Tice, 1997). In certain areas
dipping has been carried out for over a century, making it difficult for cattle herds to
reach endemic stability to TBD, especially as calves are also dipped (Norval et al.,
1983). This prevents calves from developing a natural immunity by being exposed to the
parasites when they are relatively resistant to Babesia infections (Norval et al., 1983).
Gray and de Vos (1981) found no evidence of Babesia bovis during a serological survey
in the Northern Province of South Africa. De Vos and Potgieter (1983) reported that
Babesia bigemina was present on 26 farms in the Northern Transvaal but they found no
evidence of Babesia bovis during their survey. However, Sutherst (1987a) used a
climatic model, CLIMEX, in South Africa, and singled out Venda as a possible area
where Boophilus microplus might successfully become established.
The study area is endemic for Babesia bigemina, but over the past 15 years Babesia
bovis has established itself in the eastern part of the Soutpansberg and Venda Districts of
the Northern Province. Clinical outbreaks of Asiatic redwater (Babesia bovis infection)
were reported from Venda in the mid-1980s (Loock, 1999, personal communication;
Gous, 1999, personal communication). In Venda, redwater is mainly transmitted during
the rainy season (October to May) when Boophilus numbers are high (De Vos, 1979).
Only 10 % of the 144 cases of redwater confirmed in Venda between 1997 and 1999
(Fig. 1. 1) were recorded during winter. Most of the confirmed cases (74 %) were due to
Babesia bovis (Loock, 1999, personal communication). Other clinical cases were
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probably not reported by the farmers and it was presumed that the actual mortality rate
due to redwater was much higher (Loock, 2000, personal communication).
Redwater Disease, 1997, 1998, 1999
50
Nu mb er o f clin ical cas es
45
40
35
30
1997
25
1998
20
1999
15
10
5
0
B. bigemina
B. bovis
Fig. 1. 1. Confirmed cases of bovine babesiosis in the study area in 1997, 1998 and
1999.
1. 4. The main objectives of this study were:
•
To confirm the presence of Boophilus microplus in the Soutpansberg,
Dzanani, Mutale, Thohoyandou and Vuwani Districts in the Northern
Province of South Africa and to determine its geographical distribution
within this area.
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•
To determine the serological prevalence of Babesia bovis and Babesia
bigemina in a representative sample from cattle in the same districts.
•
To determine the relative number of Boophilus microplus in relation to
Boophilus decoloratus and to establish if any displacement of Boophilus
decoloratus by Boophilus microplus is taking place.
•
To map the distribution of Boophilus decoloratus and Boophilus
microplus in the study area in the Northern Province and to attempt to
model the findings, using the CLIMEX model, to predict possible further
spread of Boophilus microplus.
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CHAPTER 2. LITERATURE REVIEW
2. 1. The genus Babesia
2. 1. 1. Comparative morphology and strain differences.
•
Babesia bigemina is a large Babesia, up to 5µm x 3 µm in size, occurring
singly or in pairs in erythrocytes. Single forms are elongated or clubshaped; in pairs the angle between the merozoites is typically acute
(Hoyte, 1976; Potgieter, 1977; Potgieter and Els, 1977; Levine, 1985).
•
Babesia bovis is a small Babesia, up to 2.4µm x 1.5 µm in size, and one
or two parasites are found in each erythrocyte (Neitz, 1941). Single
Babesia bovis organisms are round, oval or irregular in shape, while
paired forms are club shaped, sometimes with rounded ends. The angle
between the paired organisms is often, but not always, obtuse (Hoyte,
1976; Potgieter, 1977; Levine, 1985).
•
Strain differences and antigenic variation in Babesia species. Several
researchers (Neitz, 1941; Riek, 1964; Callow, 1964; 1967; 1968;
Johnston and Tammemagi, 1969; Curnow, 1973a; Doyle, 1977;
Thompson et al., 1977; De Vos, 1978; Mahoney et al., 1979a; Smith et
al., 1980; Callow et al., 1981) found evidence of immunological strain
differences in both Babesia bigemina and Babesia bovis. Immunological
differences between strains from different geographical locations have
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also been demonstrated with Babesia bigemina and Babesia bovis
(Mahoney, 1974). Hall (1963) showed that when calves were challenged
with a strain of Babesia bigemina other than that to which they had
acquired passive immunity from their dams, the disease reaction was
almost as severe as experienced by calves from fully susceptible mothers.
Recovered cattle were also more resistant when challenged with the
homologous strain when compared to heterologous strains (Callow, 1967;
1968; Johnston and Tammemagi, 1969; Smith et al., 1980).
The strains differ in virulence, and frequent cyclic transmission may
cause this to increase (Callow, 1984). Some Australian strains of Babesia
bigemina are relatively non-pathogenic (Johnston, 1968; Mahoney, 1974;
James et al., 1985). Antigenic differences within a Babesia bovis strain
are often found, and these revert to a common, strain-specific type after
being transmitted through the tick vector Boophilus microplus (Curnow,
1973a). Cross-immunity is common between different strains in infected
animals (Mahoney et al., 1979a; Mahoney et al., 1979b).
2. 1. 2. Diagnosis of redwater. Parasites are detected in appropriately stained peripheral
blood smears by light microscopy, positive identification of the parasites under the
microscope being the only way to confirm a presumptive diagnosis. Babesia bovis can
also be detected in organ smears, particularly those made from brain tissue at necropsy
(De Vos and Potgieter, 1994).
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2. 1. 3. Geographical distribution in South Africa.
•
Babesia bovis was probably reported for the first time in South Africa
from the Cape Colony in 1905 (Potgieter and Els, 1977). In 1941 it was
identified in Pretoria (Neitz, 1941) and was later recorded in coastal
KwaZulu-Natal and Mpumalanga (De Vos, 1979; De Vos and Potgieter,
1983), and subsequently from the interior of KwaZulu-Natal (De Vos
and Every, 1981). The known distribution of Babesia bovis is shown in
Fig. 2. 1.
• Babesia bigemina is indigenous to southern Africa (Lawrence and
Norval, 1979) and has been recorded in KwaZulu-Natal, Mpumalanga,
Gauteng, the Northern Province and in large parts of the North West
Province. It also occurs in parts of the Eastern Cape Province, the coastal
parts of the Western Cape Province, parts of the Free State Province and
in the north-eastern corner of the Northern Cape Province (De Vos,
1979). The known distribution of Babesia bigemina is shown in Fig. 2. 1
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Fig. 2. 1. Map showing the geographical distribution of Babesia bigemina and Babesia
bovis in South Africa (adapted from De Vos, 1979; De Vos and Every, 1981; De Vos
and Potgieter, 1983; Jagger et al., 1985; Wedderburn et al., 1991).
2. 1. 4. Transmission by the vectors.
•
Babesia bigemina is transmitted to cattle by the one-host ticks Boophilus
decoloratus and Boophilus microplus (Riek, 1964; Potgieter, 1977;
Potgieter and Els, 1977; Norval et al., 1983; Callow, 1984) and to a much
lesser extent by the two-host tick Rhipicephalus evertsi evertsi (Büscher,
1988). The importance of Rhipicephalus evertsi evertsi as a vector of
Babesia bigemina in the field is uncertain (Howell et al., 1978).
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Adult female Boophilus decoloratus and Boophilus microplus ticks
acquire the Babesia bigemina infection in the final stage of feeding; the
infection is then passed transovarially to the larvae. The life cycle of each
tick species is identical (Potgieter and Els, 1977). The larvae that hatch
are infected but not infective; the sporozoites are transmitted to cattle by
both nymphs and adults of the Boophilus species. The Babesia bigemina
infection in Boophilus species is retained by transovarial transmission in
the absence of reinfection from a susceptible host for at least two
generations (Callow, 1965; Potgieter, 1977; Potgieter and Els, 1977; Gray
and Potgieter, 1981; Dalgliesh and Stewart, 1983; Büscher, 1988).
Nymphs of Rhipicephalus evertsi evertsi have been thought to transmit
Babesia bigemina, although with difficulty (Neitz, 1941; Büscher, 1988).
•
Babesia bovis is transmitted by Boophilus microplus, the only known
vector in southern Africa (Riek, 1966; Potgieter, 1977). The female tick is
infected when engorging, and the infection is passed transovarially to the
larvae. The larvae then transmit the sporozoites to cattle whilst feeding
but clear themselves of the infection and neither nymphs nor adults
transmit the infection (Potgieter, 1977; Potgieter and Els, 1979; Mahoney
and Mirre, 1979; Gray and Potgieter, 1981; Dalgliesh and Stewart, 1983).
The Babesia bovis infection is not transmitted to the next generation of
ticks without going through its life cycle in the vertebrate host (Mahoney
and Mirre, 1979).
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2. 1. 5. Clinical signs of the diseases.
•
African redwater. Clinical signs of bovine babesiosis caused by Babesia
bigemina begin 7-21 days after the initial attachment of an infected tick
(Callow and Dalgliesh, 1982). The first sign is usually a temperature
exceeding 40°C, coupled with anorexia. The animal is depressed with
haemoglobinuria as a consistent finding shortly after the onset of the
disease. A clinically detectable anaemia soon develops and the animal
may die if not treated. In more protracted cases there is marked icterus
(Callow et al., 1993; De Vos and Potgieter, 1994). Babesia bigemina
infection is normally eliminated from the cattle within 6 months (Callow
et al., 1974b).
•
Asiatic redwater. The clinical signs of bovine babesiosis caused by
Babesia bovis are similar to those of Babesia bigemina but the disease is
more acute, has a shorter course with more severe signs and a higher
mortality rate. Animals are weak and reluctant to move; they have an
increased respiratory rate, fever and severe depression. At this stage
haemoglobinuria is not usually present but diarrhoea is common and
pregnant cattle may abort. Signs of central nervous system (CNS)
involvement develop in some animals and manifest as nystagmus,
circling, head pressing, aggression, convulsions and paralysis. The
mortality rate is higher than that of African redwater and in nonfatal cases
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the recovery period is protracted (Smith et al. 1980; Norval et al., 1992b;
Callow et al., 1993; De Vos and Potgieter, 1994; Bock et al., 1997).
Cattle which survive the acute disease become persistent carriers of the
infections for periods of 1-4 years during which they show no clinical
evidence of being infected (Mahoney, 1969; Callow, 1977). Babesia
bovis infections can persist for 1-4 years and ticks feeding on the carriers
can become infected (Johnston and Tammemagi, 1969; Mahoney et al.,
1973)
2. 1. 6. Pathogenesis of bovine babesiosis. The most important factor in bovine
babesiosis is the invasion and breakdown of the erythrocytes by the parasites
(McCosker, 1981). Haemolytic anaemia is a feature of both diseases, although in
Babesia bovis infections acute cases may die before evidence of clinical anaemia
develops (De Vos and Potgieter, 1994). The acute haemolytic phase lasts for about a
week (Callow, 1977) and toxins and by-products of tissue necrosis can lead to serious
clinical abnormalities (Callow, 1984).
2. 1. 7. Pathology.
•
Babesia bigemina. There is rapid intravascular haemolysis and the serum
haemoglobin levels are high, giving rise to haemoglobinuria. Kidney
damage is usually evident and the kidneys are enlarged with degeneration
of the convoluted tubules. The liver undergoes fatty degeneration and the
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gall bladder contains large amounts of bile. The spleen is enlarged. The
carcass is anaemic with watery blood and pulmonary oedema a regular
feature. Icterus is common in animals with the chronic form of the
disease (Callow, 1977; Callow et al., 1993; De Vos and Potgieter, 1994).
•
Babesia bovis. Findings are similar to but more severe than with Babesia
bigemina infection as proteolytic enzymes are released by the
erythrocytes and coagulation is disturbed. There are also anoxic
degenerative changes in the blood vessels of the brain, liver, kidneys and
skeletal muscles. The cerebral cortex often shows a pink discoloration
that is pathognomonic for the disease. Acute cases may die before any
anaemia is noticed, although severe anaemia may develop in the more
protracted cases. The post mortem examination shows intense congestion
of most organs and icterus is seen in those cases which survive the initial
disease (Smith et al., 1980; Callow and Dalgliesh, 1982; Callow, 1984;
Callow et al., 1993; De Vos and Potgieter, 1994).
2. 1. 8. Immunity.
•
General immunity. Previously unexposed adult cattle of all breeds
develop severe disease on first infection with Babesia species (Trueman
and Blight, 1978; De Vos and Potgieter, 1994; Bock et al., 1997).
Mortality from Babesia bovis in susceptible herds can be as high as 50 –
80 % (Callow, 1977; Norval et al., 1992a; Bock et al., 1997). Babesia
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bovis infection may persist in Bos taurus cattle for at least four years, and
the immunity acquired by those cattle which eliminate the infection
without treatment, may persist even longer. If the cattle are challenged
regularly, this resistance will persist for the rest of their lives (Callow,
1967, 1968; Mahoney, 1969; Mahoney et al., 1973; Johnston et al., 1978;
Trueman and Blight, 1978; Mahoney et al., 1979b). The degree of
acquired immunity to Babesia bovis is influenced by the degree of
exposure to the parasite (Callow et al., 1974a). Immunity in calves that
are naturally infected before the age of 5-7 months with both Babesia
bigemina and Babesia bovis may also persist for at least four years
(Mahoney et al., 1973; Johnston et al., 1978; Mahoney et al., 1979b).
Mortality from Babesia bigemina can be as high as 5-10 % if susceptible
cattle are brought into an endemic area (De Vos, 1979). Cattle clear
themselves of Babesia bigemina infection within a period lasting from a
few months to as long as two years, but can retain a sterile immunity
(Callow, 1967; Mahoney, 1969; Löhr, 1972; Callow et al., 1974b;
Johnston et al., 1978). An infection with Babesia bigemina can give some
cross-protection against Babesia bovis but the reverse has not been
demonstrated (Wright et al., 1987).
•
Age-dependent immunity. Age-dependent immunity allows the animal
to become infected with the parasite without succumbing to disease
(Riek, 1968). When a cow has been infected with Babesia bovis or
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Babesia bigemina, she will produce antibodies to these parasites. Newborn calves will absorb the antibodies secreted in the colostrum and be
immune against infection against the homologous strain for 7-360 days,
with a mean of 119 days (Hall, 1963; Hall et al., 1968; Ross and Löhr,
1970; Callow, 1984). This immunity is sterile unless the calves become
infected with the parasite (Hall, 1963; Ross and Löhr, 1970); the duration
of such immunity depends on the amount of antibodies the calves have
ingested (Riek, 1968). Should calves in this state of passive immunity
become infected they generally do not manifest clinical signs but develop
an acquired immunity (Latif et al., 1979; Dallwitz et al., 1986). Calves
born to non-immune dams are susceptible to clinical disease (Hall, 1963),
until an age-specific immunity takes over at 2-4 months and persists until
the calf is 9 months of age (Riek, 1963; Trueman and Blight, 1978;
Callow, 1984). This immunity is not dependent on the dam’s
immunological status (Callow, 1977; Riek, 1968; Mahoney and Ross,
1972; Mahoney, 1974; Mahoney et al., 1979b).
• Breed-dependent immunity. Bos indicus cattle develop a relatively high
degree of immunity after exposure to Babesia bovis, compared to that of
Bos taurus cattle (Daly and Hall, 1955; Francis, 1966; Bigalke et al.,
1976; Johnston et al., 1978; Johnston et al., 1981; Callow, 1984; James
et al., 1985; Rechav and Kostrzewski, 1991; Bock et al., 1997; 1999a).
Bos indicus cattle have a lower level of Babesia bovis parasitaemia
compared to Bos taurus cattle which are similarly infected (Johnston,
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1967; Bock et al., 1997). In Bos taurus calves the passively acquired
immunity to Babesia bovis does not prevent subclinical infection, while
in Bos indicus calves such immunity may persist for several months and
might in fact contribute to a potentially unstable situation by interfering
with active immunization (Mahoney, 1974). Bos indicus cattle and their
crosses rid themselves of patent parasitaemia sooner than Bos taurus
breeds and after a while the parasite can no longer be detected in the
blood (Johnston et al., 1978). A similar difference has not been observed
with Babesia bigemina (Johnston, 1967; Mahoney et al., 1973; Callow et
al., 1974b). Under similar environmental conditions a Bos indicus-cross
herd will have a lower rate of Babesia bovis transmission than a Bos
taurus herd, and therefore needs a higher level of tick infestation to
maintain endemic stability (Mahoney, 1979).A breed-dependent
immunity to Babesia bigemina is less clear (Bock et al., 1999b). Daly
and Hall (1955) and Johnston (1967) found comparable immunological
reactions to Babesia bigemina in different cattle breeds but De Vos
(1979) and Bock et al. (1999b) found crossbred Bos indicus and Bos
indicus steers significantly more resistant to Babesia bigemina than Bos
taurus cattle. Resistance in Bos indicus varies according to the virulence
of the parasite and, under similar conditions, Bos taurus cattle were
found to be more susceptible to the clinical disease (Bock et al., 1999b).
Jongejan et al. (1988) observed a low incidence of African redwater
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outbreaks in Zambia and concluded that this may have been due to the
innate resistance of the local cattle breeds (Perry et al., 1984).
2. 1. 9. Endemic stability to redwater. When redwater is first introduced into an area,
cattle are highly susceptible to the disease, and a mortality rate of up to 40% has been
reported in untreated Hereford cattle suffering from Babesia bovis infection (Callow,
1977; Trueman and Blight, 1978). De Vos (1979) reported mortality rates of 5 – 10 % in
outbreaks of Babesia bigemina infections in South Africa. Endemic stability to both
Babesia bigemina and Babesia bovis develops, but a stable situation for one Babesia
species does not necessarily imply a stable situation for the other (De Vos, 1979). In
Zimbabwe dipping was disrupted for a number of years and endemic stability to TBD
developed rapidly after the initial heavy losses of nearly one million cattle. Subsequent
losses were minimal (Norval, 1982; Norval et al., 1983).
The maintenance of an endemically stable situation is dependent on a regular supply of
ticks infected with Babesia bigemina and/or Babesia bovis. When the tick challenge is
high a large number of infected ticks feed on the hosts, and there is a steady inoculation
of the parasite (Callow, 1984). Young animals are protected by their age-specific
immunity and are generally exposed to infection before the age of 9 months. Further
repeated exposures to infected ticks ensure that a high level of antibodies is maintained
in the animals and endemic stability develops. An infection rate in calves close to 100 %
at the age of 9 months would indicate that endemic stability has been reached (Mahoney
and Ross, 1972; Callow, 1977).
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Norval et al. (1992b) defined endemic stability as “a climax relationship between host,
vector and environment in which all co-exist with the virtual absence of clinical disease,
while endemic instability means an incomplete relationship (between host, vector and
environment) in which clinical disease occurs”. In Zimbabwe Norval et al. (1983)
described five different epidemiological situations for bovine babesiosis:
•
Endemically stable situations (81 – 100 % positive sera)
•
Situations approaching endemic stability (61 – 80 % positive sera)
•
Endemically unstable situations (21 – 60 % positive sera)
•
Minimal disease situations (1 – 20 % positive sera)
•
Disease–free situations (0 % positive sera)
In an endemically stable region most of the calves would have seroconverted to Babesia
bovis and/or Babesia bigemina by 9 months of age. Low infection rates in cattle over 9
months can lead to endemic instability and a risk of outbreaks of disease (Mahoney and
Ross, 1972). Endemic stability can, however, be disrupted by intensive dipping or a
change in climatic conditions (Bigalke et al., 1976; De Vos, 1979; Norval, 1982;
Callow, 1984). Cattle grazing for long periods on crop residue land, seasonal movement
of herds in search of fresh grazing or abnormally cold winters may interrupt or delay
transmission of TBD in the young animals and cause endemic instability (Dallwitz et al.,
1986). Boophilus ticks rarely survive for longer than 6 months on pastures in the
absence of hosts, and rotational grazing may prevent the young animals from reaching
endemic stability to TBD (Bigalke et al., 1976; Ardington, 1982).
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2. 2. The tick vectors of bovine babesiosis in southern Africa.
Boophilus microplus has a worldwide distribution and is found in Asia, Australia,
Central and South America, West Indies and parts of Africa. Boophilus decoloratus is
found throughout Africa and is common in southern Africa (Brown et al., 1990).
2. 2. 1. Boophilus species on domestic and wild animals in southern Africa.
•
Boophilus decoloratus (African blue tick) is a one-host tick and one of
the most common cattle ticks in South Africa. It has a wide host range but
cattle are the main domestic animal hosts, while dogs, horses and
donkeys also can be heavily infested (Theiler, 1962; Mason and Norval,
1980). Sheep and goats are also suitable hosts (Walker et al., 1978).
Wild animals can become infested with this tick, with Burchell’s zebra
(Equus burchelli), blue wildebeest (Connochaetes taurinus), black
wildebeest (Connochaetes gnou), giraffe (Giraffa camelopardalis),
African buffalo (Syncerus caffer), bushbuck (Tragelaphus scriptus), kudu
(Tragelaphus
strepsiceros),
nyala
(Tragelaphus
angasi),
eland
(Taurotragus oryx), impala (Aepyceros melampus), grey rhebok (Pelea
capreolus) and warthog (Phacochoerus aethiopicus) sometimes carrying
quite heavy burdens (Horak, 1982; Horak et al., 1983; Horak et al., 1984;
Horak et al., 1986; Horak et al., 1988).
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• Boophilus microplus (Asiatic cattle tick, pan tropical blue tick) is a onehost tick and cattle are the main hosts but it has also been found on other
domestic animals such as sheep, goats, dogs and horses (Smith, 1983).
Wild animals are rarely hosts of this tick (MacLeod and Mwanaumo,
1978; Walker, 1991; Boomker et al., 1983), but it has been collected off
lion (Panthera leo), grey rhebok, sable antelope (Hippotragus niger),
grey duiker (Sylvicapra grimmia) and African buffalo. There are
indications that its potential range is similar to that of Boophilus
decoloratus (Theiler, 1962; Horak et al., 1986; Walker, 1991).
2. 2. 2. Characteristics of the genus Boophilus. Boophilus species can be identified by
the presence of an inornate scutum, a hexagonal basis capitulum, short mouth-parts, pale
yellow legs, small eyes, absence of festoons, and the presence of anal plates in the male
(Gothe, 1967a; Arthur and Londt, 1973; Howell et al., 1978; Walker et al., 1978).
2. 2. 3. Comparative morphology. Boophilus decoloratus is difficult to distinguish
from Boophilus microplus (Gothe, 1967a). Macroscopically, males and females of
Boophilus decoloratus are somewhat lighter brown in colour than Boophilus microplus
and the body of the Boophilus decoloratus female tends to be a little larger and more
elongated than that of Boophilus microplus. The semi-engorged female Boophilus
microplus is rounder with a slimmer “waist”. Microscopically the principal features used
for identification are the shape of the mouthparts of both males and females (Howell et
al., 1978; Wedderburn et al., 1991). Boophilus decoloratus has three rows of denticles
on each side of the hypostome and a convex protuberance with setae on the medial
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aspect of the first palpal segments (Arthur and Londt, 1973). Boophilus microplus has
four rows of denticles on each side of the hypostome and a concavity with no setae on
the medial aspect of the first palpal segment.
The males of Boophilus decoloratus have long adanal plates, which reach beyond the
posterior body margin and the long internal spurs are clearly visible outside the scutum.
In Boophilus microplus the adanal plates do not reach beyond the posterior body margin
and they have a short internal spur and an even shorter external spur (Gothe, 1967a;
Arthur and Londt, 1973; Heyne, 1986).
2. 2. 4. Geographical distribution and seasonal incidence of Boophilus decoloratus
and Boophilus microplus in southern Africa. The conditions for survival of both
Boophilus decoloratus and Boophilus microplus are ideal over large areas of southern
Africa (Theiler, 1962; McCosker, 1981). The two species occur together in many parts
of the subcontinent, but because Boophilus microplus has more specific climatic
requirements, Boophilus decoloratus has the wider distribution (De Vos, 1979).
Temperature and precipitation (Theiler, 1962; Gothe, 1967b; De Vos, 1979) limit the
spread of both ticks. The prevalence of both tick species seems to decline at higher
altitudes in South Africa (Baker et al., 1989), whilst Boophilus decoloratus is found in
large numbers at higher altitude zones in Zimbabwe (Lawrence and Norval, 1979;
Mason and Norval, 1980), Zambia (MacLeod and Mwanaumo, 1978), and Kenya (Gitau
et al., 1997).
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2. 2. 4. 1. Distribution of Boophilus decoloratus in southern Africa. Boophilus
decoloratus can survive in areas where there is a maximum of 90 days of frost spread
over a period of 150 days a year (Gothe, 1967b). At lower temperatures there may be
pockets of suitable climatic conditions where it can survive and develop (Theiler, 1949;
Gothe, 1967b). The tick can survive in areas with an annual rainfall as low as 380 mm
(Walker et al., 1978; De Vos, 1979), and it can tolerate even lower rainfall if the area is
covered by bush rather than by open grassland (Theiler, 1949; Walker et al., 1978).
Decreasing humidity seems to be the limiting factor in the tick’s distribution (Theiler,
1949; Gothe 1967b).
•
Boophilus decoloratus in South Africa. The climatic conditions in South
Africa are not harsh enough to restrict the spread of Boophilus
decoloratus, but cold conditions and low rainfall may limit its numbers
and activity (Theiler, 1949; Gothe, 1967b; Rechav, 1982). In South
Africa Boophilus decoloratus is widely distributed in the Northern
Province, Gauteng, Mpumalanga and the eastern part of the North-West
Province as well as KwaZulu-Natal. It also occurs in the northern and
eastern part of the Free State Province, the northeastern and eastern parts
of the Eastern Cape Province and in the southern coastal belt and winter
rainfall areas of the Western Cape. It is absent from the desert shrub of
Karoo veld, Namaqualand and the northwestern part of the Eastern Cape
Province (Theiler, 1949; 1962; Baker and Ducasse, 1967; Londt et al.,
1979; Robertson, 1981; Rechav, 1982; Walker, 1991; Dreyer et al.,
1998a).
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Boophilus decoloratus is present throughout the year in those areas where
it normally occurs in South Africa (Baker and Ducasse, 1967; Robertson,
1981; Rechav, 1982). The main period of activity is from November to
June, with peaks in July, September-October, December-January and
March-April (Baker and Ducasse, 1967; Howell et al., 1978; Londt et al.,
1979; Robertson, 1981; Rechav, 1982; Baker et al., 1989; Spickett et al.,
1989; Rechav and Kostrzewski, 1991; Tice, 1997). The evidence suggests
that its life cycle probably has two to four generations per annum
(Rechav, 1982; Rechav and Kostrzewski, 1991; Dreyer et al., 1998a).
Peaks were found in late autumn (March to May) and in winter (June to
August) in the Free State Province, where a survey demonstrated that
nearly 80 % of the annual Boophilus burden occurred during the cooler
months of the year (Dreyer et al., 1998a)
•
Boophilus decoloratus in Zimbabwe. The tick is present in most regions
of the country but is more common in the higher rainfall eastern part of
Zimbabwe (Theiler, 1962; Lawrence and Norval, 1979; Mason and
Norval, 1980; Norval et al., 1983). It is absent in those areas of the
country which have been cleared of wild and domestic ungulates due to
tsetse fly control, and small populations only are found in the dry southwestern lowveld (Mason and Norval, 1980). Boophilus decoloratus is
present in Zimbabwe throughout the year without exhibiting distinct
seasonal peaks, and is thought to have an annual seasonal cycle of two to
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four generations (Jooste, 1966; Matson and Norval, 1977; Mason and
Norval, 1980).
•
Boophilus decoloratus in Zambia. The tick is widely distributed in the
central, southern and western parts of Zambia (Theiler, 1962; MacLeod
and Mwanaumo, 1978; Pegram et al., 1986). It can survive in the hot and
dry Luangwa Valley, where Boophilus microplus is absent, and in the
cooler and wetter high-altitude areas in other districts (MacLeod and
Mwanaumo, 1978). There are two periods of abundance in Zambia
(March to July and September to December) and the tick probably
completes two to five generations per year (MacLeod, 1970; Pegram et
al., 1986).
•
Boophilus decoloratus in Swaziland. The tick is widespread in
Swaziland (Theiler, 1949; Jagger et al., 1985; Walker, 1991; Wedderburn
et al., 1991).
•
Boophilus decoloratus in Mozambique. Boophilus decoloratus is
probably present throughout the country (Theiler, 1962).
•
Boophilus decoloratus in Botswana. The tick is mainly present along the
eastern and south-eastern agricultural strip on the border with South
Africa and Zimbabwe as well as in the Okavango Delta and in the northeastern Chobe District (Theiler, 1962; Walker et al., 1978; Walker,
1991).
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•
Boophilus decoloratus in Namibia. The tick occurs from the thornveld
of Damaraland in the north to Windhoek in the south and it has also been
collected in Ovamboland, Okavango and in the Caprivi Strip (Theiler,
1962; Biggs and Langenhoven, 1984; Walker, 1991).
2. 2. 4. 2. Distribution of Boophilus microplus in southern Africa. Boophilus
microplus prefers warm and humid conditions and can survive in areas where there is a
maximum of 60 days of frost, spread over a period of 150 days a year (Gothe, 1967b).
The larvae are susceptible to cold and can only tolerate 0° C for 72 hours. Cold seems to
be the limiting factor in the tick’s distribution (Gothe, 1967b; De Vos, 1979). It is not
known how tolerant adults are of cold. Temperatures must be at least 15-20° C for egg
laying and larval hatching to occur, with a maximum upper threshold of 40 °C. The
relative humidity must be at least 80 % for eggs to survive (Callow, 1984; Sutherst and
Maywald, 1985), and the tick is absent in areas with annual rainfall of less than 500 mm
(De Vos, 1979). The seasonal changes seem to be similar to those of Boophilus
decoloratus (Arthur and Londt, 1973; De Vos, 1979; Baker et al., 1989).
•
Boophilus microplus in South Africa. Cold conditions seem to have
restricted the spread of Boophilus microplus in South Africa (Gothe,
1967a). The first recorded report of Boophilus microplus in South Africa
was in 1908 when Howard stated that it was present in the southeastern
districts of the then Cape Province (Theiler, 1962). In the survey by
Theiler (1962), Boophilus microplus was found in the mild and humid
coastal strip between Bredasdorp and Port Elizabeth where rainfall occurs
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all year round. More recent surveys have indicated that Boophilus
microplus is present in northern Gauteng, parts of Mpumalanga, large
areas of KwaZulu-Natal, parts of the Eastern Cape Province and along
the southern Cape coast (Howell et al., 1978; De Vos, 1979; Baker et al.,
1989; Walker, 1991). The main periods of seasonal activity are similar to
Boophilus decoloratus (De Vos, 1979).
•
Boophilus microplus in Zimbabwe. Boophilus microplus was probably
introduced from Mozambique in the mid-1970s (Mason and Norval,
1980; Norval et al., 1992a) when it was restricted to the eastern and
northern part of the country. Boophilus microplus was later found close to
the South African border, and there was serological evidence of Babesia
bovis in the area (Mason and Norval, 1980; Norval et al., 1983). The
population dynamics are similar to those of Boophilus decoloratus
(Mason and Norval, 1980; Norval et al., 1983). After the drought of
1981-1984 Boophilus microplus was thought to have disappeared
completely from Zimbabwe (Norval, unpublished data, cited by Norval et
al., 1992a). However, Babesia bovis antibodies were detected in the
eastern and northern parts of Zimbabwe and Boophilus microplus was
collected in the eastern and north-western part of the country (Katsande et
al., 1996). Boophilus microplus is probably still present in these areas
(Katsande et al., 1999) and its presence in the south-eastern lowveld
indicated that the tick could survive in most areas of Zimbabwe (Mason
and Norval, 1980).
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•
Boophilus microplus in Zambia. Boophilus microplus was first recorded
in northern Zambia (Theiler, 1962), whilst MacLeod and Mwanaumo
(1978), Pegram et al. (1986) and Berkvens et al. (1998) reported that it
was widely distributed in the eastern and northern sector of the country,
where it had partially or totally displaced Boophilus decoloratus. The tick
was found at intermediate altitudes in hot and dry areas where it would be
expected to be absent in light of current knowledge of the tick’s climatic
requirements (Berkvens et al., 1998). Two patterns of seasonal
abundance were present: in areas with low Boophilus microplus numbers
peaks were recorded in April-May and in August. Four generations per
year were found in areas with high tick numbers (Berkvens et al., 1998).
•
Boophilus microplus in Swaziland. Boophilus microplus was first
recorded in Swaziland during a survey in 1985 after a series of outbreaks
of bovine babesiosis caused by Babesia bovis (Jagger et al., 1985). Its
distribution in Swaziland is patchy, but it is present throughout the
country (Wedderburn et al., 1991).
•
Boophilus microplus in Mozambique. The tick is presumably present
throughout Mozambique (Theiler, 1962), although definite reports on the
distribution of the tick in this country are difficult to access.
•
Boophilus microplus in Namibia. The tick has not been recorded in
Namibia (Walker, 1991).
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•
Boophilus microplus in Botswana. The tick has not been recorded in
Botswana (Walker et al.1978; Walker, 1991).
2. 2. 5. Interbreeding and competition between Boophilus species. Shortly after the
introduction of Boophilus microplus into South Africa researchers stated that the tick (as
Boophilus fallax, Howard, 1908; as Boophilus annulatus, Dönitz, 1910) was ousting
Boophilus decoloratus from the latter’s endemic areas (Theiler, 1962). Observations in
the field of mixed infections of Boophilus decoloratus and Boophilus microplus revealed
that, where the two species co-existed, there was a tendency for Boophilus microplus to
displace Boophilus decoloratus partially or totally (MacLeod and Mwanaumo, 1978;
Mason and Norval, 1980; Norval et al., 1983; Norval and Short, 1984; Norval and
Sutherst, 1986; Sutherst, 1987b; Wedderburn et al., 1991; Berkvens et al., 1998; Baker,
2001, personal communication).
This displacement is rapid and Boophilus microplus can completely displace Boophilus
decoloratus in 4-10 generations, which would generally take 1-3 years to complete
(Sutherst, 1987b). Several authors, who argued that it could be related to climatic
factors, reproductive capability, interspecific competition on the host, adaptation to the
environment and different resistance patterns to acaricides, have discussed the potential
mechanisms for the displacement.
Boophilus decoloratus is more tolerant of low temperatures and dry conditions than
Boophilus microplus (Theiler, 1949; Gothe, 1967b). Arthur and Londt (1973) described
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a shorter life cycle for Boophilus microplus than for Boophilus decoloratus. Spickett and
Malan (1978) found that the two species were genetically incompatible as cross-matings
produced sterile eggs. As Boophilus females mate once only (Londt, 1976), crossmatings would result in decreased Boophilus fertility. In areas where both species were
present, their numbers were low, possibly because of this cross-mating tendency (Baker
et al., 1989).
The replacement of Boophilus decoloratus by Boophilus microplus seemed only to a
small degree to be due to reproductive competition. Norval and Sutherst (1986) showed
that the cross-matings were not random events, but that there was a tendency for
assortative mating (i.e. each species will mate with their own species if this is possible)
to occur. As a result there were fewer hybrid matings than would be expected if mating
was random. Hilburn and Davey (1992) doubted these results and concluded that due to
different development times of the two species, the number of assortative matings was
probably higher.
The attatchment sites on the animal are similar for both species (Howell et al., 1978).
Norval and Short (1984) found that Boophilus microplus fed more successfully on cattle
than did Boophilus decoloratus and more females of Boophilus microplus completed
feeding and continued their developmental stages on cattle. The presence of Boophilus
microplus on cattle appears to enhance their resistance to Boophilus decoloratus: a
reduction in engorged weight resulted in Boophilus decoloratus females producing
fewer eggs, which contributed to a decrease in their population. Interspecific
competition on the host was the most likely explanation for the displacement of
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Boophilus decoloratus by Boophilus microplus (Norval and Short, 1984). Boophilus
decoloratus would probably not be present where Boophilus microplus is already well
established (Norval et al., 1983).
Sutherst (1987b) showed in a computer model that the displacement was due to
reproductive interference combined with faster population growth rates by Boophilus
microplus. In warm, high rainfall areas this gave Boophilus microplus an advantage over
Boophilus decoloratus of 3.5 in terms of population growth potential. In colder and drier
areas with a resident wild ungulate population acting as a host reservoir for Boophilus
decoloratus, the advantage was negligible and here Boophilus decoloratus would
probably persist (Sutherst, 1987b).
Mason and Norval (1980) described a similar pattern of displacement in Zimbabwe, and
suggested that the displacement of Boophilus decoloratus by Boophilus microplus may
be due to changing environments, such as changes in weather patterns, or development
of acaricide resistance by Boophilus microplus. In Zimbabwe displacement did take
place in the absence of dipping as well as in areas where widly differing climate and
weather conditions occurred.
In Zambia, MacLeod and Mwanaumo (1978) found that Boophilus decoloratus had been
displaced by Boophilus microplus in large areas in the Central Province. Berkvens et al.
(1998) found Boophilus decoloratus still present in areas with low stocking rates,
indicating that less intense competition between the species favoured Boophilus
decoloratus.
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Where Boophilus decoloratus and Boophilus microplus occur together, their relative
resistance to acaricides is uncertain. Baker et al. (1968) reported greater resistance of
Boophilus microplus larvae to some acaricides, but from later trials it was concluded that
Boophilus microplus was more susceptible to the most commonly used acarides than
Boophilus decoloratus (Solomon et al., 1979; Baker et al., 1981).
2. 2. 6. Infection rates of Babesia species in Boophilus species. The infection rate can
be defined as the proportion of tick larvae (Babesia bovis) or nymphs and adults
(Babesia bigemina) harbouring the Babesia. The transmission of Babesia parasites to
susceptible cattle is dependent on the proportion of ticks harbouring Babesia combined
with the ability of these ticks to pass on the infection to cattle (Mahoney, 1974).
2. 2. 6. 1. Observed Babesia bigemina and Babesia bovis infections in ticks. Riek
(1964; 1966) found infections of Babesia bovis and Babesia bigemina in Boophilus
microplus of 90 % when the tick had fed on cattle with tick-transmitted infections.
Johnston (1967) reported that Babesia bigemina infection in Boophilus microplus ranged
from 2-10 % whilst Babesia bovis infections ranged from 0.06-0.47 %. Mahoney and
Mirre (1971) recorded that 0.5-14 % of Boophilus microplus larvae contained Babesia
bovis whilst 20-40 % contained Babesia bigemina. Mohammed (1976) found Babesia
bigemina infections in Boophilus decoloratus that varied between 2 and 10 %. Gray and
Potgieter (1981) reported close to 30 % of Boophilus decoloratus ticks infected with
Babesia bigemina. By using Polymerase Chain Reaction (PCR), Smeenk et al. (2000)
found that 5 % of Boophilus decoloratus were positive for Babesia bigemina while 60 %
were positive for Babesia bovis. With Boophilus microplus the infection was even
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University of Pretoria etd – Tonnesen, M (2005)
higher, with 69 % of the ticks being positive for Babesia bovis. Smeenk et al. (2000)
were also able to demonstrate simultaneous infections with both Babesia bigemina and
Babesia bovis. The Babesia DNA was extracted from the haemolymph. These findings,
however, do not imply that the parasite can undergo further development in the salivary
gland of the tick and thus become infective to cattle. There is strong experimental and
epidemiological evidence that Boophilus microplus is the only vector of Babesia bovis
in southern Africa (Potgieter, 1977; Potgieter and Els, 1979; Norval et al., 1983).
2. 6. 6. 2. Infectivity of ticks to cattle. Riek (1964) suggested that the majority of
parasites ingested by a tick die, and that only a very small proportion undergoes further
development. The infection rates of Babesia species in Boophilus ticks decrease as the
ticks and the Babesia parasites go through developmental stages, with the result that the
subsequent ability of ticks to transmit the infection is low. Studies by Mahoney and
Mirre (1971) and Mahoney et al. (1981) showed that the infection of Babesia bovis in
Boophilus microplus larvae was as low as 0.04-0.07 %. The infection of Babesia
bigemina in Boophilus microplus larvae and nymphs was higher at 0.23 % (Mahoney
and Mirre, 1971). Dallwitz et al. (1986) gave infection rates of these immature stages for
Babesia bovis of 0.03 % and those for Babesia bigemina of 0.1-0.5 %. With such low
prevalence of infection in the ticks the chance of animals becoming infected was also
low (Callow, 1984). Nevertheless, only one infected tick is required to transmit Babesia
bigemina or Babesia bovis to susceptible cattle (Mahoney and Mirre, 1971).
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2. 2. 7. Environmental factors affecting the Babesia parasites in the tick. A number
of different environmental factors, tick strains, methods of infection and parasite density
in the vertebrate host can affect the development of the Babesia parasites in the tick
(Riek, 1964; 1966; Mahoney et al., 1981). The development of both Babesia bigemina
and Babesia bovis in Boophilus microplus was slower at temperatures below 20° C
(Riek, 1963; 1964; 1966), whilst higher temperatures stimulated the development
(Dalgliesh and Stewart, 1979; 1982; Dalgliesh et al., 1979; Ouhelli and Schein, 1988).
Riek (1966; 1968) found that different strains of Boophilus microplus had different
susceptibilities to infection with Babesia bovis, and heavy Babesia infections as well as
virulent Babesia bovis strains could result in tick mortality (Riek, 1966, 1968; Dalgliesh
et al., 1981; Callow, 1984). If the infection rate of Babesia bigemina and Babesia bovis
in the host is too high, the engorged females will die (Riek, 1964; 1966).
2. 2. 8. Inoculation rate. This rate is a measure of the average daily probability that an
animal in a herd will become infected with babesiosis (Mahoney and Ross, 1972;
Mahoney, 1974). The inoculation rate (h) can be defined as the number of tick bites (m)
received by the host per day, multiplied by the proportion of the vector population
carrying infective forms of the organism (a) and the proportion of bites that successfully
infect the host (b) (Mahoney, 1974). The formula to calculate the inoculation rate is:
h = mab
In this model the number of ticks biting each animal per day is important and the higher
the inoculation rate, the higher the number of calves infected whilst being protected by
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age-specific resistance. In an endemically stable situation the inoculation rate ranged
from 0,005 to 0,05, depending on the number of ticks in the field (Mahoney, 1979). A
minimum number of Boophilus tick bites to maintain endemic stability in a herd of
exotic cattle would be at least 20 bites per day. Bos indicus cattle, however, had a higher
level of resistance against Babesia bovis than Bos taurus cattle and would need a
minimum of 40 tick bites a day to maintain stability (Mahoney et al., 1981). Smith
(1983) used a computer model to calculate the number of Boophilus ticks necessary to
maintain endemic stability and suggested 8-9 engorged ticks/day as the optimal number.
Jongejan et al. (1988) calculated inoculation rates in calves in the range of 0.05-0.3 %
for Babesia bovis and 0.3-0.6 % for Babesia bigemina and concluded that the situation
seemed endemically unstable, but that there were no disease outbreaks. The age-specific
prevalence rates, however, indicated endemic stability, (Jongejan et al., 1988).
2. 2. 9. Breed resistance against Boophilus species. There are major differences
between Bos indicus and Bos taurus breeds in their resistance to Boophilus spp.
(Bonsma, 1981; Hewetson, 1981). Under similar environmental conditions Bos indicus
cattle were infested with lower numbers of ticks (Johnston, 1967; Mahoney, 1979;
Sutherst and Comins, 1979; Sutherst et al., 1979; Bonsma, 1981; Mahoney et al., 1981;
Kaiser et al. 1982; Rechav and Zeederberg, 1986; Rechav and Kostrzewski, 1991;
Fourie et al., 1996). The resistance in cattle is related to the thickness of the skin, the
amount of subcutaneous muscles, the mobility of the cow’s tail and the quality of the
coat, all of which prevent the ticks from becoming attached and engorging fully
(Francis, 1966; Bonsma, 1981). The numbers of ticks on Bos indicus and Bos
indicus/Bos taurus crossbreeds were significantly less than on purebred Bos taurus cattle
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(Francis, 1966; Utech et al., 1978; Bonsma, 1981; Sutherst and Utech, 1981; Norval et
al., 1992b). Crosses with Zebu-type cattle seem to have particular resistance-building
qualities (Sutherst and Utech, 1981; Spickett et al., 1989).
2. 2. 10. Other factors affecting host resistance against Boophilus species. An
infection with Babesia bovis can cause immunosuppression against Boophilus
microplus; and Callow and Stewart (1978) demonstrated that calves infected with
Babesia bovis had a larger tick burden than uninfected calves. The Babesia parasite thus
improves its chance of survival and transmission by increasing the number of its vectors,
its prevalence being related to vector density (Callow and Stewart, 1978). Malnutrition
reduces the resistance to ticks (O’Kelly and Seifert, 1969) and factors such as lactation,
sex and age may affect resistance (Utech et al., 1978; Sutherst and Utech, 1981). It
appears that some animals have an innate resistance to ticks as they consistently carry
fewer ticks than others do in the same group (Sutherst et al., 1979; Petney et al., 1990;
Latif et al., 1991; Dreyer et al., 1998b). Resistance to a new tick species starts
developing as soon as cattle are challenged and will increase after prolonged exposure.
The resistance is proportional to the degree of tick challenge (Utech et al., 1978).
When calves become infested with Boophilus microplus it might take as long as 2 years
before their level of resistance stabilizes. Calves normally carry lighter tick burdens than
adult cattle as tick infestations have been found to be nearly three times higher on their
dams. This suggests that young animals might be protected by some age-related
resistance (Mahoney, 1979; Sutherst et al., 1979). Prolonged tick challenge later in life
further promotes host resistance against ticks (Sutherst and Utech, 1981). Excessive
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grooming and close proximity between individuals can lead to a transfer of Boophilus
spp. between animals (Sutherst et al., 1979) and this may be a mode of transfer when
Boophilus microplus invades a new area (Mason and Norval, 1981).
2. 3. The role of models in tick control.
Computer models have been constructed to highlight the relationship between
environmental factors and tick ecology and are used to predict the potential distribution
of various tick species (Sutherst and Maywald 1985, 1986; Sutherst, 1987a; Sutherst et
al., 1991; Sutherst et al., 1995; Sutherst, 1998). Models can be used to develop a holistic
approach to a tick-parasite-host system and to decide on the best approach to combat
disease in different parts of the world (Dallwitz et al., 1986).
2. 3. 1. CLIMEX. This computer-based system allows the prediction of the possible
distribution and survival of a tick species, using known biological and climatical data
(Sutherst and Maywald, 1985; Sutherst, 1987a). The model is used in an attempt to
predict population growth during favourable and unfavourable seasons. An “Ecoclimatic
Index” (EI) is derived which indicates the climatic favourability for the location of a tick
species. The index runs from 0 to 100 and with a low EI, there is a greater likelihood of
endemic instability. An EI of less than 20 indicates that the tick is not well suited to the
environment, and the tick population will be low in that area. Transmission of TBD in
these areas would be intermittent (Dallwitz et al., 1986; Sutherst and Maywald, 1986).
In areas where the EI is less than 5, ticks will not be able to heavily parasitize cattle. In
these areas endemic stability may not be maintained, but it may be possible to eradicate
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a tick species or vaccinate against TBD. A high EI normally identifies areas that may be
permanently occupied by the tick (Sutherst and Maywald, 1985; Sutherst, 1987a).
The index is derived from a population growth index that shows the potential for an
increase in the population, and four stress indices which describe the negative effects of
extreme cold, dry, hot and wet conditions (Sutherst and Maywald, 1985). If the stress
indices reach 100, they exclude persistence of the species in that environment (Sutherst,
1998). When dryness is the limiting factor, however, the presence of local swamps or
irrigation may provide favourable habitats for the tick species even if the EI is low
(Sutherst and Maywald, 1985).
2. 3. 2. Earlier predictions using the CLIMEX model. Sutherst and Maywald (1985)
used the CLIMEX model to predict the possible spread of Boophilus microplus into new
areas in South Africa. At that stage the tick had not been found in the Soutpansberg
region, but there were indications that Babesia bovis was present (Sutherst and
Maywald, 1985; Sutherst, 1987a; Gous, personal communication, 1999).
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CHAPTER 3. MATERIALS AND METHODS
3. 1 Survey areas.
The survey area was in the Soutpansberg, Dzanani, Mutale, Thohoyandou and Vuvani
Districts in the Northern Province of South Africa and the survey was carried out
between May 1999 and December 2000. The region was chosen because of recent
outbreaks of bovine babesiosis caused by Babesia bovis (Loock, personal
communication, 1999). The area borders the Kruger National Park (KNP) to the east,
Zimbabwe to the north, the Vivo-Dendron road (R 521) to the west and the PietersburgGiyani road (R 81) to the south. Sibasa and Louis Trichardt are the administrative
centres of the veterinary services in this area. The communal farming areas were divided
into different wards, which were each serviced by an animal health technician who
would normally oversee the dipping. Five commercial farms and 30 communal dip tanks
were included in the survey.
ZIMBABWE
Messina
BOTSWANA
Sibasa
Louis Trichardt
Kruger
National
Park
NORTHERN PROVINCE
Pietersburg
Fig. 3. 1. Map of the Northern Province of South Africa showing the survey area.
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3. 1. 1. The communal farming areas. There were several dip tanks in each ward and
each dip tank serviced the cattle in an area with a maximum radius of 20 km. The cattle
belonged to several farmers and were maintained under traditional methods of animal
husbandry. They were periodically taken on set days to the communal plunge-type dip
tanks in order to control ectoparasites. The cattle dipped at the communal dip tanks
situated in these areas were mostly indigenous cattle breeds or a mix of indigenous and
exotic breeds. They were mainly kept for meat production, but were also milked for
home consumption for most of the year. They usually grazed on unfenced communal
land during the day and were not fed concentrates, but were allowed access to harvested
maize fields when available. The pastures were moderately to heavily overgrazed and
the animals were held in kraals at night with little or no housing facilities. No
vaccination against Babesia bigemina or Babesia bovis was undertaken in the area. The
cattle were not marked with ear-tags so individuals were not readily identifiable for
repeated sampling.
Compulsory dipping was practised for many years (Bigalke et al., 1976) and the cattle
had been dipped regularly at weekly or fortnightly intervals. During 2000, however, the
government subsidies for acaricides were discontinued and the farmers were expected to
pay for the acaricide. Due to the poor economic conditions and serious flooding during
February and March 2000, dipping had been discontinued in some areas and became
irregular in others. Prior to 1996 Triatix (Amitraz + Ca-hydroxide, Intervet) was widely
used, but all the dip tanks were using Grenade (Cyhalothrin, Intervet) at the time of the
study.
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3. 1. 1. 1. Location of the different communal dip tanks.
Thononda. Geographic co-ordinates: 22° 52’ 52,2” S; 30° 15’ 13,7” E. Nine hundred
cattle were usually dipped at this dip tank.
Dzondo. Geographic co-ordinates: 23 ° 02’ 39.0’’ S; 30 ° 21’ 56.2’’ E. Three hundred
and fifty cattle were usually dipped at this dip tank.
Guyuni. Geographic co-ordinates: 22° 48’ 07.2’’ S; 30° 31’ 43.7’’ E. Eight hundred
cattle were usually dipped at this dip tank and 25% were young animals
Sendedza. Geographic co-ordinates: 22 ° 54’ 17.6’’ S; 30 ° 11’ 04.2’’ E. Nine hundred
cattle were usually dipped at this dip tank.
Luvhanga. Geographic co-ordinates: 23 ° 01’ 05.5’’ S; 30 ° 31’ 00.9’’ E. Fourteen
hundred cattle were usually dipped at this dip tank.
Muledzhi. Geographic co-ordinates: 22 ° 41’ 23.7’’ S; 30 ° 37’ 07.8’’ E. Six hundred
cattle were usually dipped at this dip tank and 25 % were young animals.
Malavuwe. Geographic co-ordinates: 22 ° 52’ 12.4’’ S; 30 ° 37’ 58.6’’ E. Eight hundred
cattle were usually dipped at this dip tank and 25 % were young animals.
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Makwarani. Geographic co-ordinates: 22° 51’ 26.4 S; 0° 24’ 36.3’’ E. Six hundred
cattle were usually dipped at this dip tank and 15% were young animals. The cattle were
in poor condition and there had been excessive mortality in the calves due to internal
parasites.
Lamvi. Geographic co-ordinates: 22° 39.2’ S; 30° 47.3’ E. Seven hundred cattle were
usually dipped at this dip tank and 25 % were young animals.
Tshaulu. Geographic co-ordinates: 22° 48’ 24,5” S; 30° 45’ 04,4” E. Six hundred cattle
were usually dipped at this dip tank and 20-25 % were young animals.
Davhana. Geographic co-ordinates: 23° 12.6’ S; 30° 28.6’ E. Fifteen hundred cattle
were usually dipped at this dip tank.
Mahagala. Geographic co-ordinates: 22° 45’ 52,1” S; 30° 51’ 09,4” E. Six hundred
cattle were dipped weekly at this dip tank and 25 % were young animals.
Matshena. Geographic co-ordinates: 22° 28’ 11.9’’ S; 30° 36’ 46.6’’ E. Nine hundred
cattle were dipped fortnightly at this dip tank.
Phipidi. Geographic co-ordinates: 22° 56’ 41,9” S; 30° 24’ 16,0” E. Two hundred and
thirty cattle were dipped every second week at this dip tank.
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Shakadza. Geographic co-ordinates: 22° 36’ 48,6” S; 30° 32’ 59,7” E. Eight hundred
cattle were dipped every second week at this dip tank.
Fesekraal 1. Geographic co-ordinates: 22° 24’ 04.4’’ S; 30° 35’ 04.4’’ E. Two hundred
cattle were dipped every second week at this dip tank.
Matatani. Geographic co-ordinates: 22° 32’ 44,3” S; 30° 44’ 37,7” E. Nine hundred
cattle were usually dipped at this dip tank. The dip tank was located in a dry area, but
some of the cattle herds grazed on the southern slopes of the Soutpansberg Mountains
where there were favourable conditions for tick survival.
Tshiendeulu. Geographic co-ordinates: 22° 49’ 20,3” S; 30° 11’ 06,7” E. Six hundred
and fifty cattle were usually dipped at this dip tank.
Khakhu. Geographic co-ordinates: 22° 50’ 16,3” S; 30° 15’ 19,4” E. Twelve hundred
cattle were usually dipped at this dip tank.
Murangoni. Geographic co-ordinates: 22° 54’ 23,4” S; 30° 23’10,8” E. Two hundred
and seventy cattle were usually dipped at this dip tank.
Gondeni. Geographic co-ordinates: 22° 54’ 39,2” S; 30° 26’ 33,2” E. Six hundred cattle
were usually dipped at this dip tank.
Savhani. Geographic co-ordinates: 22° 40’ 41,1” S; 30° 30’13” E. Twelve hundred
cattle were dipped at this dip tank and they were dipped every second or third week.
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Tshikotoni. Geographic co-ordinates: 22° 39’ 34,3” S; 30° 26’ 41,7” E. Eleven hundred
cattle were dipped every second week and 15-20 % were young.
Mphephu. Geographic co-ordinates: 22 ° 52’ 22.1’’ S; 30 ° 06’ 37.7’’ E. A
thousand cattle were usually dipped at this dip tank.
Keerweerder. Geographic co-ordinates: 22 ° 42’ 34.2’’ S; 30 ° 11’ 01.0 ’’ E. Six
hundred cattle were usually dipped at this dip tank and they were a mixture of
Afrikander and Brahman breeds.
Masetoni. Geographic co-ordinates: 22 ° 42’ 52.0’’ S; 30 ° 53’ 18.7’’ E. Two hundred
and eighty cattle were usually dipped at this dip tank.
Fripp. Geographic co-ordinates: 22 ° 48’ 36.3’’ S; 29 ° 57’ 01.5’’ E. Three hundred and
seventy cattle were usually dipped at this dip tank.
Maunguwi. Geographic co-ordinates: 22° 49’ 51.8’’ S; 30° 03’ 34.8’’ E. Three hundred
and eighty cattle were usually dipped at this dip tank.
Sambandou. Geographic co-ordinates: 22° 44.2’ S; 30° 39.6’ E. Nine hundred and fifty
cattle were usually dipped at this dip tank.
Makonde Project. Geographic co-ordinates: 22° 46’ 38.2’’ S; 30° 32’ 38.0’’ E. One
hundred and twenty cattle were usually dipped at this dip tank.
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3. 1. 1. 2. Vegetation types and climatic conditions at the dip tanks. Two major veld
types were found in the research area, namely Sour Lowveld Bushveld and
Soutpansberg Arid Mountain Bushveld (Acocks, 1975; Low and Rebelo, 1996). A few
of the dip tanks were situated in Mopani Bushveld and Mixed Lowveld Bushveld.
•
Sour Lowveld Bushveld. This vegetation type was found mainly on the
lower eastern slopes of the Soutpansberg Mountains at altitudes between
550 and 800 m. The annual rainfall in the area varied from 600 to 1000
mm, and temperatures varied from 2 ° C to 43 ° C with an average of
22 ° C. The soil types varied from deep sandy soils at the higher
altitudes to more clay-like soils derived from granites and gneisses in
the lower areas. Riverine forests and open tree savanna vegetation were
common. Common trees and shrubs in the area included silver
clusterleaf (Terminalia sericea), bushwillow (Combretum collinum),
paperbark thorn (Acacia sieberiana), common hook-thorn (Acacia
caffra), common wild fig (Ficus thonningii) and spineless monkey
orange (Strychnos madagascariensis). In the shrub layer sickle bush
(Dichrostachys cinerea), large sourplum (Ximenia caffra) and camel’s
foot (Piliostigma thinningi) were found. The common grasses consisted
of yellow thatching grass (Hyperthelia dissoluta), common thatchgrass
(Hyparrhenia hirta) and wiregrass (Elionurus muticus).
The dip tanks which were located in this vegetation zone were
Thononda,
Dzondo,
Guyuni,
Sendedza,
Luvhanga,
Muledzhi,
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Malavuwe,
Makwarani,
Lamvi,
Tshaulu,
Mahagala,
Phipidi,
Tshiendeulu, Khakhu, Murangoni, Gondeni, Tshikotoni, Masetoni,
Sambandou and Makonde Project.
• Soutpansberg Arid Mountain Bushveld. This vegetation type was
found on the dry, hot, rocky northern slopes and summits of the
Soutpansberg Mountains at altitudes between 300 and 2050 m. The
annual rainfall in the area varied from 300 mm in the north to 500 mm
on the plateau, and temperatures varied from 3 ° C to 44 ° C, with an
average of 23 ° C. The soil was mainly acidic sandy, loamy and gravelly
soil derived from sandstone, quartzite and shale. The main trees in this
area were white seringa (Kirkia acuminata), red bushwillow
(Combretum apiculatum), common hook-thorn, red seringa (Burkea
africana), silver clusterleaf
and Lebombo ironwood (Androstachys
johnsonii). The shrubs included spineless monkey orange, velvet
sweetberry (Bridelia mollis), redheart tree (Hymenocardia ulmoides)
and shakama plum (Hexalobus monopetalus). Guinea grass (Panicum
maximum), common fingergrass (Digitaria eriantha) and tassel threeawn (Aristida congesta) were common grasses in the area.
The dip tanks that were located in this vegetation type included
Matshena, Shakadza, Matatani, Savhani, Mphephu, Keerweerder, Fripp
and Maunguwi.
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• Mopani Bushveld. This vegetation type was located from the KNP to the
Soutpansberg, to the north of the mountains and into Zimbabwe at
altitudes between 300 and 700 m. The rainfall in the area varied from
250 to 550 mm per year, and the temperatures varied from 1.5 ° C to
42.5 ° C with an average of 22 ° C. The soil types varied from sandy
and clay-like soils in the KNP to sandstone, shale and basalt north of the
Soutpansberg and in the Limpopo Valley. Mopane (Colophospermum
mopane), red bushwillow, knob thorn (Acacia nigrescens) and baobab
(Adansonia diditata) were the most common trees. The shrub layer
consisted of wild raisin bush (Grewia spp.), three-hook thorn (Acacia
senegal), small sourplum (Ximenia americana) and other Ximenia spp.
The
common
grasses
consisted
of
common
nine-awn
grass
(Enneapogon cenchroides), tassel three-awn, Kalahari sand quick
(Schmidtia pappophoroides) and Panicum spp.
Fesekraal was the only dip tank located in this vegetation type.
•
Mixed Lowveld Bushveld. This vegetation type was found on flat and
undulating landscapes at altitudes between 350 and 500 m. The annual
rainfall in the area varied from 450 to 600 mm and the temperatures
varied from – 4 ° C to 45 ° C, with an average of 22 ° C. The soil was
sandy and clay-like in the higher parts, with a high sodium content in the
lower parts. The vegetation was dense and bushy with open savanna in
the low-lying areas and forest along the riverbanks. Common trees and
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bushes were red bushwillow, largefruit bushwillow (Combretum zeyheri)
and silver clusterleaf. In the more low-lying places knobthorn, scented
thorn (Acacia nilotica) and common falsethorn (Albizia harveyi) were
found. The shrub layer consisted of hairy corkwood (Commiphora
africana), wild grape (Cissus cornifolia) and sickle bush. The grass layer
was poorly to moderately developed and among the grasses found were
herringbone grass (Pogonarthria squarrosa), blueseed grass (Tricholaena
monachne) and curlyleaf lovegrass (Eragrostis rigidor). Grasses such as
Kalahari sand quick, spreading bristlegrass (Aristida congesta) and
bushveld signalgrass (Urochloa mosambicensis) were also common.
Davhana was the only dip tank located in this vegetation type.
3. 1. 2. The commercial farming areas. The cattle on the commercial farms were
mostly beef breeds which were bred for commercial sale, but also included some dairy
breeds and stud animals. The breeds commonly found were Simmentaler, Friesian,
Afrikander, Nguni, Jersey, Bonsmara and Brahman. On some of the farms the older
cattle had been vaccinated against Babesia bovis and Babesia bigemina and these
animals were not included in the serological testing. Some farmers had dip tanks and
spray races on the premises, but hand spraying, hand-dressing and pour-ons were also
used. Grazing on the farms was abundant and the cattle were in good condition.
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3. 1. 2. 1. Detailed description of the five commercial farms.
•
Zwartrandjes Farm. Geographic co-ordinates: 29 ° 52’ E; 23 ° 14’ S.
This farm was owned by Mr. A. MacDonald and carried 160 Bonsmara
cattle, 60 of which were younger than 12 months. The average annual
rainfall on the farm was 400-500 mm but during 2000 the farm received 3
times the normal rainfall and serious flood damage occurred (MacDonald,
personal communication, 2000). The cattle were checked daily for any
signs of disease and clinical cases of redwater were treated with Berenil
(Diminazene, Intervet). Babesia bovis had never been diagnosed on the
farm. The tick burden on the farm was low and consisted mainly of
Rhipicephalus appendiculatus, Amblyomma hebraeum and Boophilus
species. The cattle were rotated between camps every two weeks. Certain
camps, which were heavily shaded, appeared to carry more ticks than
open camps (MacDonald, personal communication, 1999). The cattle
were spray-dipped with Ektoban (Cymiazol + Cypermethrin, Bayer
Animal Health) once a week in summer and every third week or more in
winter.
The herd was semi-closed and a certain number of new bulls were
brought in every year. The 18-month-old weaners were usually only
vaccinated against Babesia bigemina. Due to the unusually heavy rainfall
in 2000, the farmer vaccinated all the calves under 6-7 months against
both Babesia bigemina and Babesia bovis as a precautionary measure.
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Consequently, serological testing on this farm was discontinued but tick
collection was continued to determine whether Boophilus microplus was
present.
•
Modderfontein Farm. Geographic co-ordinates: 29° 53’ E; 23° 29’ S.
This farm was owned by Mr. F. Oldreive and carried 570 cattle, most of
which were Friesians, Bonsmara or Simbra, which is a mixture of
Simmentaler and Brahman. The annual rainfall on the farm was 800-900
mm. Clinical cases of both African and Asiatic redwater had occurred on
the farm and the incidence was highest in the age group 18-24 months.
Fourteen clinical cases of Asiatic redwater were recorded in 1999
(Oldreive, personal communication, 2000). The tick burden was heavy
and Boophilus were the most common tick species on the cattle.
Five camps were grazed only by the heifers, five by the beef animals and
seven by the dairy cattle. The heifer camps carried the heaviest tick
burdens and the heifers were first allowed to graze in these camps at the
age of 9-10 months. The cattle were hand-sprayed with Tikgard
(Chlorfenvinphos + alphamethrin, Pfizer Animal Health) once a week in
summer and once every three weeks in winter. Bayticol (Flumethrin,
Bayer Animal Health) and Paracide (Alphamethrin, Pfizer Animal
Health) were found to be ineffective, probably due to resistance
(Oldreive, personal communication, 1999). The herds were semi-closed
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with only the bulls being brought in annually. The herds had never been
vaccinated against bovine babesiosis.
•
Nooitgedacht Farm. Geographic co-ordinates: 30 ° 04’ E; 23 ° 08’ S.
The farm was owned by Mr. P. Ahrens and carried 250 Simmentaler stud
cattle, of which 70 were younger than 12 months. Cattle were vaccinated
against both Babesia bovis and Babesia bigemina when they were 2 years
old. The management on the farm was good and the cattle were checked
for disease and ticks on a regular basis. The cattle were kept nearly free of
ticks. Although bovine babesiosis almost never occurred on the farm, 20
deaths due to Babesia bovis had recently been confirmed (Ahrens,
personal communication, 1999).
The cattle were plunge-dipped and after the outbreak of bovine babesiosis
the owner chose to switch to Ektoban. The farm was later omitted from
the survey due to low levels of ticks and low prevalence of antibodies to
TBD. Tick control was strict and the cattle were dipped as soon as ticks
appeared. The low prevalence of antibodies in the animals under 2 years
was probably due to the vaccination of older cattle.
•
Mara Research Station. Geographic co-ordinates: 29° 25’ E; 23° 6’ S.
The herd consisted of 800 cattle which were mainly Bonsmara,
Simmentaler, Afrikander, Nguni and Jersey crosses and 250 of them were
younger than 12 months. The average annual rainfall was 450 mm but
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University of Pretoria etd – Tonnesen, M (2005)
during the very wet year in 2000 double this amount was received.
Babesia bigemina was present at Mara and had previously caused
mortalities. The tick burden was low and consisted mainly of
Amblyomma species, although during 2000 a heavier than normal
Boophilus burden was recorded.
Two hundred camps were divided equally among the 15 herds and
specific camps were allocated to each herd. The cattle were plungedipped with Ektoban when there were more than an average of 10 adult
Amblyomma hebraeum per animal on a sample selected from each herd
(Du Plessis et al., 1992).
About 100 cattle were added to the station every year as replacements.
These cattle were dipped on arrival, isolated for some weeks and then
dipped again before they were introduced to the resident herd. In 2000, 60
cattle were tested for antibodies to Babesia species, but due to the
structured camp system a random sample could not be taken. The serum
samples were omitted from the survey in 2000, but tick collection was
continued to determine whether Boophilus microplus was present.
•
Naboomkop Farm. Geographic co-ordinates: 30° 20’ E; 23° 09’ S. This
farm was owned by Mr. S. Wilson and carried 150 adult cattle and 50
young animals. The breeds were Brahman and Brahman x Bonsmara. The
annual rainfall on the farm was 700 mm but in 2000 the farm received
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University of Pretoria etd – Tonnesen, M (2005)
1500 mm. Newly introduced cattle had recently succumbed to bovine
babesiosis, and this was suspected to be an important cause of mortality
among the young calves. Sick animals were not treated. The tick burden
was heavy at times with abundant Boophilus species present but the
burden was lighter than normal during the first half of 2000.
The farm was divided into several camps, and the camps that were most
commonly used had the heaviest tick burdens (Wilson, personal
communication, 1999). The cattle were hand-sprayed once a week with
Pro-dip (Cypermethrin, Logos Agvet), Paracide and Bayticol. Triatix
(Amitraz, Intervet) was not used as the farmer felt it was ineffective
(Wilson, personal communication, 1999). The herd was open, and adult
cows were added at irregular intervals. One or two bulls were brought in
every year and 30 of the cows in the herd had been brought in as adults.
3. 1. 2. 2. Vegetation types and climatic conditions on the commercial farms. The
commercial farms were located in three different vegetation type zones
(Acocks, 1975; Low and Rebelo, 1996): Sour Lowveld Bushveld, Mixed
Bushveld and Sweet Bushveld.
•
Sour Lowveld Bushveld. The commercial farms located in this
vegetation type were Nooitgedacht and Naboomkop.
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University of Pretoria etd – Tonnesen, M (2005)
•
Mixed Bushveld. This vegetation type occurred in large parts of the
Northern Province and varied from short, dense bushveld to open tree
savanna. The area consisted of plains at an altitude of 700 to 1100 m. The
rainfall varied from 350 to 650 mm per year, and temperatures varied
from –8 ° C to 40 ° C with an average of 21 ° C. The soil was coarse,
sandy and shallow, with underlying granite, quartzite, sandstone and
shale. The open tree savanna consisted of silver clusterleaf, peeling plane
(Ochna pulchra), wild raisin (Grewia flava) and red seringa (Burkea
africana). On shallow soil red bushwillow, common hook-thorn (Acacia
caffra), sicklebush and live-long (Lannea discolor) dominated the area.
The most common grasses were fingergrass (Digitaria eriantha),
Kalahari sand quick, broom grass (Eragrostis pallens) and purple spike
cat’s tail (Perotis patens).
The commercial farms located in this vegetation type were Zwartrandjes
and Modderfontein.
•
Sweet Bushveld. This vegetation type was found in the dry and hot
Limpopo River Valley and in the valleys of tributary rivers at altitudes
between 800 and 950 m. The rainfall varied from 350 to 500 mm per
year, and temperatures varied from –5 ° C to 40 ° C with an average of 21
° C. The soil is deep and sandy, covering granite, quartzite and sandstone.
The tree species most commonly found were silver clusterleaf, yellow
pomegranate (Rhigozum obovatum), wild raisin, common corkwood
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University of Pretoria etd – Tonnesen, M (2005)
(Commiphora pyracanthoides) and shepherd’s tree (Boscia albitrunca).
Dense thickets of blue thorn (Acacia erubescens), black thorn (Acacia
mellifera) and sicklebush are prominent features of this veld type. The
grasses were dominated by sweetveld species such as Kalahari sand
quick, broom grass and various Aristida species. Guinea grass, small
panicum (Panicum coloratum) and blue buffalograss (Cenchrus ciliaris)
were also common.
The commercial farm located in this vegetation type was Mara Research
Station.
3. 2. Experimental design.
3. 2. 1. Sample selection. A 2-stage non-probability cluster sampling method was used
to sample the cattle (Thrusfield, 1995). The farms/dip tanks in the Northern Province
were the primary units and the individual animals at each dip tank/farm were the
secondary sampling units. The primary units were selected by the State Veterinarian Dr.
Pieter Loock and Veterinary Technologist Mr. T. Tshisamphiri. The sampling method
was non-probability (convenience) sampling (Thrusfield, 1995), and farms/dip tanks
were selected according to the following criteria:
•
History of occurrence of Babesia bigemina/Babesia bovis.
•
Number of cattle on the dip tank/farm.
•
Geographical location.
55
University of Pretoria etd – Tonnesen, M (2005)
•
Usability of the crush.
•
Farmers’ willingness to participate in the study.
3. 2. 2. Sample population in the study area.
•
Dip tanks. The total cattle population in Dzanani, Mutale,
Thohoyandou and Vuvani districts was 103,252 heads, distributed
among 142 dip tanks (1999 South African census). The number of
cattle normally dipped at each tank varied from 200 to 1500. Based
on an estimated herd prevalence of 60 %, a sample of 30 dip tanks
would be sufficient to give 95 % confidence of being within 10 % of
the true prevalence of Babesia bovis and Babesia bigemina. Cattle
from 11 of the dip tank areas (for convenience these are referred to
merely as “dip tanks”) were selected in 1999 for inclusion in the
study. Tick collection at two of these dip tanks was continued in 2000
to monitor any changes in the Boophilus population. None of the dip
tanks were monitored for changes in serology in 2000. Nineteen new
dip tanks were added to the survey in 2000. The 30 dip tanks that
were sampled during 1999 and 2000 serviced 22,000 cattle.
•
Commercial farms. There were 595 commercial farm units in the
Soutpansberg district with a total cattle population of 128,200. The
number of cattle on the commercial farms in the survey varied from
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University of Pretoria etd – Tonnesen, M (2005)
160 to 800 per farm. Five commercial farms were selected in 1999
for inclusion in the study and two of these farms were further
monitored for changes in serology during 2000. Tick collection at
four of the commercial farms was continued in 2000 to monitor any
changes in the Boophilus population.
3. 2. 3. Blood collection. The prevalence of TBD in the survey areas was unknown, so
50 % prevalence was estimated with a desired confidence level of 95 %. (Thrusfield,
1995). The number of animals required for the serology test was calculated (Martin et
al., 1987). The unit for analysis was the individual animal. Seropositive results were
expressed as seroprevalence and defined as P = a/b where a was the number of positive
animals and b the number of animals tested (Alvarez et al., 1996).
With the exception of one dip tank where only 41 cattle were bled, 60 cattle were bled at
each dip tank and commercial farm. The animals were randomly selected according to
the number of cattle at the dip tank/farm. The sample of animals was split into 4 to 14month-old animals, and those older than 18 months. Where possible, a minimum of 30
animals in each age group was sampled.
Cattle were held in a crush prior to dipping and blood samples were taken. Blood
samples were collected from the tail vein (v. caudalis mediana) into a 10 ml. Monoject*
Vacutainer tube without anti-coagulant. The blood samples were carefully labelled,
making sure that the age group was clearly indicated. Blood could not be collected from
57
University of Pretoria etd – Tonnesen, M (2005)
the same animals at subsequent collections as most animals on the communal lands were
not marked in any way.
The blood samples were stored at room temperature for 4 hours to allow clotting, and
were then centrifuged at 3000 rpm for 20 min. The sera were decanted into 4 ml
cryotubes (Cryovial*) and stored at –10 C° at the Veterinary Laboratories at
Sibasa/Louis Trichardt. The cryotubes were clearly marked with the year, date, dip
tank/farm and age of the animal. They were later transferred on ice to the Onderstepoort
Veterinary Institute (OVI), where the serum samples were analyzed for antibodies
against Babesia bigemina and Babesia bovis using the Indirect Fluorescent Antibody test
(IFAT) (Anon., 1984).
3. 2. 4. Tick collection. The sampling method chosen for tick collection was
convenience sampling (Trushfield, 1995) to avoid injury to animals and the collectors.
At each dip tank/commercial farm six young animals, aged 4-14 months, which carried a
heavy Boophilus tick burden were sampled before dipping and care was taken to choose
cattle from different owners.
Boophilus ticks were collected from young cattle in May, September, November and
December 1999, in May, October and December 2000 and in February 2001. The ticks
were collected early in the morning so that as many replete ticks as possible could be
counted (Johnston, 1967). The calves were restrained on the ground with ropes and the
Boophilus ticks were removed by hand. Templates on certain body areas were used
when collecting the ticks and all adult ticks inside the templates were collected (Baker
58
University of Pretoria etd – Tonnesen, M (2005)
and Ducasse, 1967). Small templates (5 x 5 cm) were used on the neck, poll and dewlap
and larger templates (10 x 10 cm) on the elbow region, knee and perineum. The ticks
were preserved in 70 % ethanol and the containers were marked to indicate the name of
the dip tank, a number (1 to 6) allocated to each animal and the sampling site on the
animal.
In certain areas the tick burdens were very low and ticks from several animals were
pooled. As many ticks as possible from these locations were collected into 70 % ethanol.
The ticks were collected when the animals were held in crushes prior to dipping and
stored in containers marked to indicate the sampling date of the dip tank. No templates
were used for these collections.
In the ectoparasite laboratory in the Department of Veterinary Tropical Diseases at the
Faculty of Veterinary Science at Onderstepoort, the Boophilus ticks were identified by
the author as either Boophilus decoloratus or Boophilus microplus using a stereoscopic
microscope. The ticks were distinguished as engorged females (e.f.), unengorged
females (u.e.f), males (m.) and immatures (imm.) (Gothe, 1967a; Heyne, 1986).
3. 3. Serological procedures.
3. 3. 1. Detection of antibodies. The most widely used procedure for detection of
antibodies to Babesia species is IFAT (Joyner et al., 1972; Anon., 1984; OIE, 1996),
which is highly sensitive and specific (Anon., 1984; Todorovic and Long, 1976). In the
59
University of Pretoria etd – Tonnesen, M (2005)
routine testing done at the OVI titres over 1/80 are considered positive (Bessenger and
Schoeman, 1983).
3. 4. CLIMEX mapping.
3. 4. 1. The CLIMEX maps. The CLIMEX maps and other support were provided by
Dr. R. W. Sutherst, CSIRO Entomology, Long Pocket Laboratories, 120 Meiers Rd,
Indooroopilly, Queensland, Australia 4068. The maps were created using ArcMap 8.1
Esri Inc. software.
3. 4. 2. Climatic information. Prof. Roland Schulze, Dep. of Agricultural Engineering,
University of Natal, Pietermaritzburg, provided the climatic information. This
information included daily maximum temperatures, daily minimum temperatures,
rainfall and relative humidity collected at several sites in the Northern Province over the
past 30 years. The data were processed using CLIMEX, and Ecoclimatic Indices for
each dip tank/farm were then computed.
3. 5. Statistical analysis.
3. 5. 1. Computing of probabilities. Ms. Rina Owen and Mr. Solly Millard, University
of Pretoria, used SAS software to compute the probabilities in the survey. The Chisquare test was used to decide if the differences between sampling years, age groups and
farming models were statistically significant.
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University of Pretoria etd – Tonnesen, M (2005)
To compare the seroprevalence of Babesia bovis with that of Babesia bigemina the
Wilcoxon Rank sum test for independent samples and BMDP software was used (Keller
and Warrack, 2000).
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University of Pretoria etd – Tonnesen, M (2005)
CHAPTER 4. RESULTS
4. 1. Serological findings.
A total of 2201 blood samples were collected. With the exception of one dip tank where
only 41 cattle were bled, 60 cattle were bled at each dip tank or farm. The sample was
split into 4 to14 month-old animals, and animals older than 18 months. The results of
the serological findings are summarized in Tables 4.1- 4.14.
4. 1. 1. Seroprevalence of antibodies to Babesia bovis and Babesia bigemina
collected from cattle at the communal dip tanks during 1999 and 2000.
Seroprevalence for Babesia bovis and Babesia bigemina are given in Tables 4.1-4. 6.
Table 4. 1. Seroprevalence of antibodies to Babesia bovis and Babesia bigemina in
both age groups of cattle bled at dip tanks during 1999.
Dip tank
Babesia bigemina
No. pos.
% pos.
No. pos.
38
63.3%
19
31.7%
Thononda
Collection
date
03.05.1999
Dzondo
04.05.1999
60
43
71.7%
35
58.3%
Guyuni
05.05.1999
60
40
66.7%
37
61.7%
Sendedza
06.05.1999
60
26
43.3%
38
63.3%
Luvhanga
07.05.1999
60
44
73.3%
39
65.0%
Muledzhi
10.05.1999
60
50
83.3%
43
71.7%
Malavuwe
11.05.1999
60
30
50.0%
37
61.7%
Makwarani
12.05.1999
60
42
70.0%
37
61.7%
Lamvi
13.05.1999
60
51
85.0%
30
50.0%
Tshaulu
14.05.1999
60
33
55.0%
42
70.0%
Davhana
21.05.1999
60
21
35.0%
13
21.7%
660
418
Total
Mean
No.
tested
60
Babesia bovis
% pos.
370
63.3%
56.1%
62
University of Pretoria etd – Tonnesen, M (2005)
Table 4. 2. Seroprevalence of antibodies to Babesia bovis and Babesia bigemina in
cattle older than 18 months bled at dip tanks during 1999.
Babesia bovis
Dip tank
Thononda
Collection
date
03.05.1999
Dzondo
No. tested No. pos. % pos.
Babesia bigemina
No. pos.
% pos.
26.7%
30
20
66.7%
8
04.05.1999
30
20
66.7%
23
76.7%
Guyuni
05.05.1999
30
22
73.3%
15
50.0%
Sendedza
06.05.1999
30
12
40.0%
16
53.3%
Luvhanga
07.05.1999
30
23
76.7%
20
66.7%
Muledzhi
10.05.1999
30
28
93.3%
21
70.0%
Malavuwe
11.05.1999
30
14
46.7%
12
40.0%
Makwarani
12.05.1999
30
27
90.0%
23
76.7%
Lamvi
13.05.1999
30
22
73.3%
14
46.7%
Tshaulu
14.05.1999
30
21
70.0%
19
63.3%
Davhana
21.05.1999
30
7
23.3%
1
3.3%
330
216
Total
Mean
172
65.5%
52.1%
63
University of Pretoria etd – Tonnesen, M (2005)
Table 4. 3. Seroprevalence of antibodies to Babesia bovis and Babesia bigemina in
cattle aged 4-14 months bled at dip tanks during 1999
Babesia bovis
Dip tank
Thononda
Collection
date
03.05.1999
Dzondo
04.05.1999
30
23
76.7%
12
40.0%
Guyuni
05.05.1999
30
18
60.0%
22
73.3%
Sendedza
06.05.1999
30
14
46.7%
22
73.3%
Luvhanga
07.05.1999
30
21
70.0%
19
63.3%
Muledzhi
10.05.1999
30
22
73.3%
22
73.3%
Malavuwe
11.05.1999
30
16
53.3%
25
83.3%
Makwarani
12.05.1999
30
15
50.0%
14
46.7%
Lamvi
13.05.1999
30
29
96.7%
16
53.3%
Tshaulu
14.05.1999
30
12
40.0%
23
76.7%
Davhana
21.05.1999
30
14
46.7%
12
40.0%
330
202
Total
Mean
No.
tested
30
Babesia bigemina
No. pos.
% pos.
No. pos.
% pos.
18
60.0%
11
36.7%
198
61.2%
60.0%
64
University of Pretoria etd – Tonnesen, M (2005)
Table 4. 4. Seroprevalence of antibodies to Babesia bovis and Babesia bigemina in
both age groups of cattle bled at dip tanks during 2000.
Babesia bovis
Dip tank
Mahagala
Collection
date
02.05.2000
Matshena
03.05.2000
60
8
13.3%
2
3.3%
Phiphidi
04.05.2000
41
29
70.7%
22
53.7%
Shakadza
05.05.2000
60
50
83.3%
42
70.0%
Fesekraal 1
08.05.2000
60
6
10.0%
8
13.3%
Matatani
12.05.2000
60
36
60.0%
15
25.0%
Tshiendeulu
17.05.2000
60
46
76.7%
30
50.0%
Khakhu
24.05.2000
60
57
95.0%
55
91.7%
Murangoni
25.05.2000
60
52
86.7%
46
76.7%
Gondeni
26.05.2000
60
47
78.3%
33
55.0%
Savhani
31.05.2000
60
48
80.0%
27
45.0%
Tshikotoni
01.06.2000
60
35
58.3%
12
20.0%
Mphephu
09.10.2000
60
32
53.3%
39
65.0%
Keerweerder
10.10.2000
60
0
0.0%
20
33.3%
Masetoni
23.10.2000
60
47
78.3%
38
63.3%
Fripp
25.10.2000
60
25
41.7%
39
65.0%
Maunguwi
13.12.2000
60
47
78.3%
37
61.7%
Sambandou
14.12.2000
60
49
81.7%
31
51.7%
Makonde Project
15.12.2000
60
33
55.0%
21
35.0%
1121
700
Total
Mean
No.
tested
60
Babesia bigemina
No. pos.
% pos.
No. pos.
% pos.
53
88.3%
36
60.0%
553
62.4%
49.3%
65
University of Pretoria etd – Tonnesen, M (2005)
Table 4. 5. Seroprevalence of antibodies to Babesia bovis and Babesia bigemina in
cattle older than 18 months bled at dip tanks during 2000.
Babesia bovis
Dip tank
Mahagala
Collection
date
02.05.2000
Matshena
03.05.2000
30
6
20.0 %
2
6.7 %
Phiphidi
04.05.2000
30
23
76.7 %
19
63.3 %
Shakadza
05.05.2000
30
27
90.0 %
24
80.0 %
Fesekraal 1
08.05.2000
30
5
16.7 %
7
23.3 %
Matatani
12.05.2000
30
27
90.0 %
11
36.7 %
Tshiendeulu
17.05.2000
30
25
83.3 %
14
46.7 %
Khakhu
24.05.2000
30
28
93.3 %
27
90.0 %
Murangoni
25.05.2000
30
27
90.0 %
23
76.7 %
Gondeni
26.05.2000
30
25
83.3 %
20
66.7 %
Savhani
31.05.2000
30
25
83.3 %
10
33.3 %
Tshikotoni
01.06.2000
30
22
73.3 %
9
30.0 %
Mphephu
09.10.2000
30
22
73.3 %
15
50.0 %
Keerweerder
10.10.2000
30
0
0.0 %
10
33.3 %
Masetoni
23.10.2000
30
25
83.3 %
18
60.0 %
Fripp
25.10.2000
30
16
53.3 %
20
66.7 %
Maunguwi
13.12.2000
30
24
80.0 %
20
66.7 %
Sambandou
14.12.2000
30
19
63.3 %
14
46.7 %
Makonde Project
15.12.2000
30
15
50.0 %
10
33.3 %
570
386
Total
Mean
No.
tested
30
Babesia bigemina
No. pos.
% pos.
No. pos.
% pos.
25
83.3 %
21
70.0 %
294
67.7%
51.6%
66
University of Pretoria etd – Tonnesen, M (2005)
Table 4. 6. Seroprevalence of antibodies to Babesia bovis and Babesia bigemina in
cattle aged 4-14 months bled at dip tanks during 2000.
Dip tank
Babesia bigemina
No. pos.
% pos.
No. pos.
% pos.
28
93.3%
15
50.0%
Mahagala
Collection
date
02.05.2000
Matshena
03.05.2000
30
2
6.7%
0
0.0%
Phiphidi
04.05.2000
11
6
54.5%
3
27.3%
Shakadza
05.05.2000
30
23
76.7%
18
60.0%
Fesekraal 1
08.05.2000
30
1
3.3%
1
3.3%
Matatani
12.05.2000
30
9
30.0%
4
13.3%
Tshiendeulu
17.05.2000
30
21
70.0%
16
53.3%
Khakhu
24.05.2000
30
29
96.7%
28
93.3%
Murangoni
25.05.2000
30
25
83.3%
23
76.7%
Gondeni
26.05.2000
30
22
73.3%
13
43.3%
Savhani
31.05.2000
30
23
76.7%
17
56.7%
Tshikotoni
01.06.2000
30
13
43.3%
3
10.0%
Mphephu
09.10.2000
30
10
33.3%
24
80.0%
Keerweerder
10.10.2000
30
0
0.0%
10
33.3%
Masetoni
23.10.2000
30
22
73.3%
20
66.7%
Fripp
25.10.2000
30
9
30.0%
19
63.3%
Maunguwi
13.12.2000
30
23
76.7 %
17
56.7 %
Sambandou
14.12.2000
30
30
100.0 %
17
56.7 %
Makonde Project
15.12.2000
30
18
60.0 %
11
36.7 %
551
314
Total
Mean
No.
tested
30
Babesia bovis
259
57.0 %
Mean
47.0 %
Seropositive reactors to B. bovis were found at 29 out of 30 (97 %) dip tanks included in
the study.
Seropositive reactors to B. bigemina were found at all (100 %) of the dip tanks included
in the study.
67
University of Pretoria etd – Tonnesen, M (2005)
Year and age groups were compared with regard to the seroprevalences of Babesia
bovis and Babesia bigemina at dip tanks during 1999 and 2000. The summaries are
given in Tables 4. 7 and 4. 8.
Table 4. 7. Chi–square test of the differences in the seroprevalence of Babesia bovis
and Babesia bigemina from cattle bled at the communal dip tanks during 1999 and
2000, compared by age. (p<0.05 is significant).
B. bovis
Young 1999 compared to
Old 1999
p=0.2581
Not significant
Young 1999 compared to
B. bigemina Old 1999
p=0.0414
Significant
Young 2000 compared to
Old
2000
p=0.0002
Significant
Young 2000 compared to
Old
2000
p=0.1257
Not significant
Table 4. 8. Chi–square test of the differences in the seroprevalence of Babesia bovis
and Babesia bigemina from cattle bled at the communal dip tanks during 1999 and
2000, compared by year. (p<0.05 is significant).
B. bovis
B. bigemina
Young 1999 compared to
Young 2000
p=0.2179
Not significant
Young 1999 compared to
Young 2000
p=0.0002
Significant
Old 1999 compared to
Old 2000
p=0.4866
Not significant
Old 1999 compared to
Old 2000
p=0.8753
Not significant
All 1999 compared to
All 2000
p= 0.7078
Not significant
All 1999 compared to
All 2000
p=0.0060
Significant
The highlighted cells show a downward trend.
68
University of Pretoria etd – Tonnesen, M (2005)
4. 1. 1. 1. Seroprevalence of antibodies to Babesia bovis and Babesia bigemina
collected from cattle bled at dip tanks situated in the Sour Lowveld Bushveld veld
type during 1999.
Seroprevalence for Babesia bovis and Babesia bigemina are given in Tables 4. 9-4. 14
Table 4. 9. Seroprevalence of antibodies to Babesia bovis and Babesia bigemina in
both age groups of cattle bled at dip tanks situated in the Sour Lowveld Bushveld
veld type during 1999.
Dip tank
Babesia bigemina
No. pos.
% pos.
No. pos.
38
63.3%
19
31.7%
Thononda
Collection
date
03.05.1999
Dzondo
04.05.1999
60
43
71.7%
35
58.3%
Guyuni
05.05.1999
60
40
66.7%
37
61.7%
Sendedza
06.05.1999
60
26
43.3%
38
63.3%
Luvhanga
07.05.1999
60
44
73.3%
39
65.0%
Muledzhi
10.05.1999
60
50
83.3%
43
71.7%
Malavuwe
11.05.1999
60
30
50.0%
37
61.7%
Makwarani
12.05.1999
60
42
70.0%
37
61.7%
Lamvi
13.05.1999
60
51
85.0%
30
50.0%
Tshaulu
14.05.1999
60
33
55.0%
42
70.0%
600
397
Total
Mean
No.
tested
60
Babesia bovis
% pos.
357
66.2%
59.5%
69
University of Pretoria etd – Tonnesen, M (2005)
Table 4. 10. Seroprevalence of antibodies to Babesia bovis and Babesia bigemina in
cattle older than 18 months bled at dip tanks situated in the Sour Lowveld
Bushveld veld type during 1999.
Babesia bovis
Dip tank
Thononda
Collection
date
03.05.1999
Dzondo
No. tested No. pos. % pos.
Babesia bigemina
No. pos.
% pos.
26.7%
30
20
66.7%
8
04.05.1999
30
20
66.7%
23
76.7%
Guyuni
05.05.1999
30
22
73.3%
15
50.0%
Sendedza
06.05.1999
30
12
40.0%
16
53.3%
Luvhanga
07.05.1999
30
23
76.7%
20
66.7%
Muledzhi
10.05.1999
30
28
93.3%
21
70.0%
Malavuwe
11.05.1999
30
14
46.7%
12
40.0%
Makwarani
12.05.1999
30
27
90.0%
23
76.7%
Lamvi
13.05.1999
30
22
73.3%
14
46.7%
Tshaulu
14.05.1999
30
21
70.0%
19
63.3%
300
209
Total
Mean
171
69.7%
57.0%
70
University of Pretoria etd – Tonnesen, M (2005)
Table 4. 11. Seroprevalence of antibodies to Babesia bovis and Babesia bigemina in
cattle aged 4-14 months bled at dip tanks situated in the Sour Lowveld Bushveld
veld type during 1999.
Babesia bovis
Dip tank
Babesia bovis
Thononda
Collection
date
03.05.1999
Dzondo
04.05.1999
30
23
76.7%
12
40.0%
Guyuni
05.05.1999
30
18
60.0%
22
73.3%
Sendedza
06.05.1999
30
14
46.7%
22
73.3%
Luvhanga
07.05.1999
30
21
70.0%
19
63.3%
Muledzhi
10.05.1999
30
22
73.3%
22
73.3%
Malavuwe
11.05.1999
30
16
53.3%
25
83.3%
Makwarani
12.05.1999
30
15
50.0%
14
46.7%
Lamvi
13.05.1999
30
29
96.7%
16
53.3%
Tshaulu
14.05.1999
30
12
40.0%
23
76.7%
300
188
Total
Mean
No.
tested
30
Babesia bigemina
No. pos.
% pos.
No. pos.
% pos.
18
60.0%
11
36.7%
186
62.7%
62.0%
71
University of Pretoria etd – Tonnesen, M (2005)
Table 4. 12. Seroprevalence of antibodies to Babesia bovis and Babesia bigemina in
both age groups of cattle bled at dip tanks situated in the Sour Lowveld Bushveld
veld type during 2000.
Babesia bovis
Dip tank
Mahagala
Collection
date
02.05.2000
Phiphidi
04.05.2000
41
29
70.7%
22
53.7%
Tshiendeulu
17.05.2000
60
46
76.7%
30
50.0%
Khakhu
24.05.2000
60
57
95.0%
55
91.7%
Murangoni
25.05.2000
60
52
86.7%
46
76.7%
Gondeni
26.05.2000
60
47
78.3%
33
55.0%
Tshikotoni
01.06.2000
60
35
58.3%
12
20.0%
Masetoni
23.10.2000
60
47
78.3%
38
63.3%
Sambandou
14.12.2000
60
49
81.7%
31
51.7%
Makonde Project
15.12.2000
60
33
55.0%
21
35.0%
581
448
Total
Mean
No.
tested
60
Babesia bigemina
No. pos.
% pos.
No. pos.
% pos.
53
88.3%
36
60.0%
324
77.1%
55.7%
72
University of Pretoria etd – Tonnesen, M (2005)
Table 4. 13. Seroprevalence of antibodies to Babesia bovis and Babesia bigemina in
cattle older than 18 months bled at dip tanks situated in the Sour Lowveld
Bushveld veld type during 2000.
Babesia bovis
Dip tank
Mahagala
Collection
date
02.05.2000
Phiphidi
04.05.2000
30
23
76.7 %
19
63.3 %
Tshiendeulu
17.05.2000
30
25
83.3 %
14
46.7 %
Khakhu
24.05.2000
30
28
93.3 %
27
90.0 %
Murangoni
25.05.2000
30
27
90.0 %
23
76.7 %
Gondeni
26.05.2000
30
25
83.3 %
20
66.7 %
Tshikotoni
01.06.2000
30
22
73.3 %
9
30.0 %
Masetoni
23.10.2000
30
25
83.3 %
18
60.0 %
Sambandou
14.12.2000
30
19
63.3 %
14
46.7 %
Makonde Project
15.12.2000
30
15
50.0 %
10
33.3 %
300
234
Total
Mean
No.
tested
30
Babesia bigemina
No. pos.
% pos.
No. pos.
% pos.
25
83.3 %
21
70.0 %
175
78 %
58.3 %
73
University of Pretoria etd – Tonnesen, M (2005)
Table 4. 14. Seroprevalence of antibodies to Babesia bovis and Babesia bigemina in
cattle aged 4-14 months bled at dip tanks situated in the Sour Lowveld Bushveld
veld type during 2000.
Babesia bovis
Dip tank
Babesia bigemina
No. pos.
% pos.
No. pos.
% pos.
28
93.3%
15
50.0%
Mahagala
Collection
date
02.05.2000
Phiphidi
04.05.2000
11
6
54.5%
3
27.3%
Tshiendeulu
17.05.2000
30
21
70.0%
16
53.3%
Khakhu
24.05.2000
30
29
96.7%
28
93.3%
Murangoni
25.05.2000
30
25
83.3%
23
76.7%
Gondeni
26.05.2000
30
22
73.3%
13
43.3%
Tshikotoni
01.06.2000
30
13
43.3%
3
10.0%
Masetoni
23.10.2000
30
22
73.3%
20
66.7%
Sambandou
14.12.2000
30
30
100.0 %
17
56.7 %
Makonde Project
15.12.2000
30
18
60.0 %
11
36.7 %
281
214
Total
Mean
No.
tested
30
Babesia bovis
149
76.2 %
53.0 %
Seropositive reactors to both B. bovis and B. bigemina were found at all (100 %) of the
dip tanks situated in Sour Lowveld Bushveld during 1999 and 2000.
Year and age groups were compared with regard to the seroprevalences of Babesia
bovis and Babesia bigemina at dip tanks situated in the Sour Lowveld Bushveld during
1999 and 2000. The summaries are given in Tables 4. 15 and 4. 16.
74
University of Pretoria etd – Tonnesen, M (2005)
Table 4. 15. Chi–square test of the differences in the seroprevalence of Babesia
bovis and Babesia bigemina from cattle bled at the communal dip tanks situated in
the Sour Lowveld Bushveld veld type during 1999 and 2000, compared by age.
(p<0.05 is significant).
Young 1999 compared to
Old 1999
p=0.0700
Not significant
Young 1999 compared to
B. bigemina Old 1999
p=0.2122
Not significant
B. bovis
Young 2000 compared to
Old
2000
p=0.5971
Not significant
Young 2000 compared to
Old
2000
p=0.1979
Not significant
Table 4. 16. Chi–square test of the differences in the seroprevalence of Babesia
bovis and Babesia bigemina from cattle bled at the communal dip tanks situated in
the Sour Lowveld Bushveld veld type during 1999 and 2000, compared by year.
(p<0.05 is significant).
B. bovis
B. bigemina
Young 1999 compared to
Young 2000
Old 1999 compared to
Old 2000
All 1999 compared to
All 2000
p=0.0004
Significant
p=0.0202
Significant
p=0.0001
Significant
Young 1999 compared to
young 2000
Old 1999 compared to
Old 2000
p=0.7410
Not significant
All 1999 compared to
All 2000
p=0.1941
Not significant
p=0.0287
Significant
The highlighted cells show a downward trend.
75
University of Pretoria etd – Tonnesen, M (2005)
4. 1. 2. Seroprevalence of antibodies to Babesia bovis and Babesia bigemina
collected from cattle on the commercial farms during 1999 and 2000.
Seroprevalence for Babesia bovis and Babesia bigemina are given in Tables 4. 17-4. 22.
Table 4. 17. Seroprevalence of antibodies to Babesia bovis and Babesia bigemina in
both age groups of cattle bled on the commercial farms during 1999.
Babesia bovis
Farm
Zwartrandjes
Collection
date
13.09.1999
Modderfontein
No. tested No. pos.
% pos.
Babesia bigemina
No. pos.
% pos.
60
9
15.0%
39
65.0%
14.09.1999
60
36
60.0%
39
65.0%
Nooitgedacht
15.09.1999
60
3
5.0%
3
5.0%
Mara Res. St.
16.09.1999
60
3
5.0%
32
53.3%
Naboomkop
17.09.1999
60
6
10.0%
32
53.3%
300
57
Total
145
Mean
19.0%
48.3%
Table 4. 18. Seroprevalence of antibodies to Babesia bovis and Babesia bigemina in
cattle older than 18 months bled on commercial farms during 1999.
Babesia bovis
Farm
Zwartrandjes
Collection
date
13.09.1999
Modderfontein
14.09.1999
Nooitgedacht
No.
tested
30
No. pos.
% pos.
Babesia bigemina
No. pos.
% pos.
2
6.7%
18
60.0%
30
22
73.3%
20
66.7%
15.09.1999
30
2
6.7%
2
6.7%
Mara Res. St.
16.09.1999
30
2
6.7%
18
60.0%
Naboomkop
17.09.1999
42
5
11.9%
26
61.9%
162
33
Total
Mean
84
20.4%
51.9 %
76
University of Pretoria etd – Tonnesen, M (2005)
Table 4. 19. Seroprevalence of antibodies to Babesia bovis and Babesia bigemina in
cattle aged 4-14 months bled on commercial farms during 1999.
Babesia bovis
Farm
Zwartrandjes
Collection
date
13.09.1999
Modderfontein
No. tested No. pos.
Babesia bigemina
% pos.
No. pos.
% pos.
30
7
23.3%
21
70.0%
14.09.1999
30
14
46.7%
19
63.3%
Nooitgedacht
15.09.1999
30
1
3.3%
1
3.3%
Mara Res. St.
16.09.1999
30
1
3.3%
14
46.7%
Naboomkop
17.09.1999
18
1
5.6%
6
33.3%
138
24
Total
Mean
61
17.4%
44.2%
Seropositive reactors to both B. bovis and B. bigemina were found on all (100 %) of the
commercial farms included in the study.
Table 4. 20. Seroprevalence of antibodies to Babesia bovis and Babesia bigemina in
both age groups of cattle bled on commercial farms during 2000.
Farm
Modderfontein
Collection
date
09.05.2000
Naboomkop
16.05.2000
Total
Mean
No.
tested
60
Babesia bovis
Babesia bigemina
No. pos.
No. pos.
40
60
29
120
69
% pos.
% pos.
66.7%
18
30.0%
48.3%
39
65.0%
57
57.5%
47.5%
77
University of Pretoria etd – Tonnesen, M (2005)
Table 4. 21. Seroprevalence of antibodies to Babesia bovis and Babesia bigemina in
cattle older than 18 months bled on commercial farms during 2000.
Farm
Modderfontein
Collection
date
09.05.2000
Naboomkop
16.05.2000
Total
Babesia bovis
Babesia bigemina
No. pos.
% pos.
No. pos.
20
66.7%
6
20.0%
30
10
33.3%
20
66.7%
60
30
No.
tested
30
Mean
% pos.
26
50.0%
43.3%
Table 4. 22. Seroprevalence of antibodies to Babesia bovis and Babesia bigemina in
cattle aged 4-14 months bled on commercial farms during 2000.
Babesia bovis
Farm
Modderfontein
Collection
date
09.05.2000
Naboomkop
16.05.2000
Total
Mean
No.
tested
30
No. pos.
Babesia bigemina
% pos.
No. pos.
% pos.
20
66.7%
12
40.0%
30
19
63.3%
19
63.3%
60
39
31
65.0%
51.7%
78
University of Pretoria etd – Tonnesen, M (2005)
Year and age groups were compared with regard to the seroprevalences of Babesia
bovis and Babesia bigemina on commercial farms during 1999 and 2000. The
summaries are given in Table 4. 23 and 4. 24.
Table 4. 23. Chi–square test of the differences in the seroprevalence of antibodies
to Babesia bovis and Babesia bigemina from cattle bled at commercial farms
during 1999 and 2000, compared by age. (p<0.05 is significant).
B. bovis
B. bigemina
Young 1999 compared to
Old 1999
p=0.5121
Not significant
Young 1999 compared to
Old 1999
p=0.1864
Not significant
Young 2000 compared to
Old 2000
p=0.0965
Not significant
Young 2000 compared to
Old 2000
p=0.3607
Not significant
Table 4. 24. Chi–square test of the differences in the seroprevalence of antibodies
to Babesia bovis and Babesia bigemina from cattle bled at commercial farms
during 1999 and 2000, compared by year. (p<0.05 is significant).
B. bovis
Young 1999 compared to
Young 2000
Old 1999 compared to
Old 2000
All 1999 compared to
All 2000
p=0.0001
Significant
p=0.0001
Significant
p=0.0001
Significant
B. bigemina Young 1999 compared to Old 1999 compared to
Young 2000
p=0.3332
Not significant
Old 2000
p=0.2596
Not significant
All 1999 compared to
All 2000
p=0.8773
Not significant
The highlighted cells show a downward trend from 1999 to 2000.
79
University of Pretoria etd – Tonnesen, M (2005)
4. 1. 3. A comparison of the seroprevalences of antibodies to Babesia bovis and
Babesia bigemina in cattle bled at communal dip tanks and commercial farms
during 1999 and 2000.
The significance values are given in Tables 4. 25 and 4. 26
Table 4. 25. Chi-square test of the differences in the seroprevalence of antibodies to
Babesia bovis and Babesia bigemina in cattle bled at the communal dip tanks and
the commercial farms during 1999 and 2000. (p<0.05 is significant).
B. bovis
Dip tanks
1999
compared to
Commercial farms 1999
p=0.0001
Significant
B. bigemina
Dip tanks
1999
compared to
Commercial farms 1999
p=0.0261
Significant
Dip tanks
2000
compared to
Commercial farms 2000
p=0.2890
Not significant
Dip tanks
2000
compared to
Commercial farms 2000
p=0.7030
Not significant
Table 4. 26. Chi-square test of the differences in the seroprevalence of antibodies to
Babesia bovis and Babesia bigemina in all cattle bled at the communal dip tanks
and the commercial farms during 1999 and 2000 compared by year. (p<0.05 is
significant).
B. bovis
B. bigemina
Young
1999
compared to
Young
2000
Old
1999
compared to
Old
2000
All
1999
compared to
All
2000
p=0.0020
significant
p=0.0001
significant
p=0.0001
significant
Young
1999
compared to
Young
2000
Old
1999
compared to
Old
2000
p=0.6804
Not significant
All
1999
compared to
All
2000
p=0.0103
Significant
The highlighted cells show a downward trend.
p=0.0366
Significant
80
University of Pretoria etd – Tonnesen, M (2005)
Differences in B. bovis seroprevalence from 1999 to 2000 when all cattle at the
communal dip tanks and commercial farms were compared. The seroprevalence to
B. bovis in the all the young cattle in the survey was significantly higher (p=0.0020) in
2000 than in 1999 (Table 4. 26). The seroprevalence in all the old cattle in the survey
was significantly higher (p=0.0001) in 2000 than in 1999. The seroprevalence to B.
bovis in all cattle in the survey was significantly higher (p=0.0001) in 2000 than in1999.
Differences in B. bigemina seroprevalence from 1999 to 2000 when all cattle at the
communal dip tanks and commercial farms were compared. The seroprevalence to
B. bigemina in the all the young cattle in the survey was significantly lower (p=0.0103)
in 2000 than in 1999 (Table 4. 26). The seroprevalence in all the older cattle in the
survey was lower in 2000 than in 1999, but the difference was not significant
(p=0.6804). The seroprevalence to B. bigemina in all cattle in the survey was
significantly lower (p=0.0366) in 2000 than in 1999.
81
University of Pretoria etd – Tonnesen, M (2005)
4. 2. Endemic stability to Babesia bovis and Babesia bigemina.
4. 2. 1. Endemic stability to Babesia bovis and Babesia bigemina in cattle at the
communal dip tanks during 1999 and 2000. The results are shown in Fig. 4. 1-4. 4.
Babesia bovis: 7 dip tanks with more than 61 % seropositive cattle:
Endemic stability or a situation approaching endemic stability
63.6 %
4 dip tanks with 21 – 60 % seropositive cattle:
Endemically unstable situation
36.4 %
0 dip tanks with 0 – 20 % seropositive cattle:
Minimal disease or disease-free situation
0.0 %
Fig. 4. 1. Endemic stability to Babesia bovis recorded at the 11 dip tanks in the
survey during 1999.
Babesia bovis: 11 dip tanks with more than 61 % seropositive cattle:
Endemic stability or a situation approaching endemic stability
57.9 %
5 dip tanks with 21 – 60 % seropositive cattle:
Endemically unstable situation
26.3 %
3 dip tanks with 0 – 20 % seropositive cattle:
Minimal disease or disease-free situation
15.8 %
Fig. 4. 2. Endemic stability to Babesia bovis recorded at the 19 dip tanks in the
survey during 2000.
82
University of Pretoria etd – Tonnesen, M (2005)
Babesia bigemina: 7 dip tanks with more than 61% seropositive cattle:
Endemic stability or a situation approaching endemic stability
63. 6 %
4 dip tanks with 21 – 60 % seropositive cattle:
Endemically unstable situation
36. 4 %
0 dip tanks with 0 – 20 % seropositive cattle:
Minimal disease or disease-free situation
0. 0 %
Fig. 4. 3. Endemic stability to Babesia bigemina recorded at the 11 dip tanks in
the survey during 1999.
Babesia bigemina: 7 dip tanks with more than 61% seropositive cattle:
Endemic stability or a situation approaching endemic stability
36.9 %
9 dip tanks with 21 – 60 % seropositive cattle:
Endemically unstable situation
47.4 %
3 dip tanks with 0 – 20 % seropositive cattle:
Minimal disease or disease-free situation
15.8 %
Fig. 4. 4. Endemic stability to Babesia bigemina recorded at the 19 dip tanks in the
survey during 2000.
83
University of Pretoria etd – Tonnesen, M (2005)
4. 2. 2. Endemic stability to Babesia bovis and Babesia bigemina recorded on the
commercial farms during 1999 and 2000. The results are shown in Fig. 4. 5-4. 8
Babesia bovis: 0 commercial farms with more than 61% seropositive cattle:
Endemic stability or a situation approaching endemic stability
0.0 %
1 commercial farm with 21 – 60 % seropositive cattle:
Endemically unstable situation
20.0 %
4 commercial farms with 0 – 20 % seropositive cattle:
Minimal disease or disease-free situation
80.0 %
Fig. 4. 5. Endemic stability to Babesia bovis recorded on the 5 commercial farms in
the survey during 1999.
Babesia bovis: 1 commercial farm with more than 61% seropositive cattle:
Endemic stability or a situation approaching endemic stability
50.0 %
1 commercial farm with 21 – 60 % seropositive cattle:
Endemically unstable situation
50.0 %
0 commercial farms with 0 – 20 % seropositive cattle:
Minimal disease or disease-free situation
0.0 %
Fig. 4. 6. Endemic stability to Babesia bovis recorded on the 2 commercial farms in
the survey during 2000.
84
University of Pretoria etd – Tonnesen, M (2005)
Babesia bigemina: 2 commercial farms with more than 61% seropositive cattle:
Endemic stability or a situation approaching endemic stability
40.0 %
2 commercial farms with 21 – 60 % seropositive cattle:
Endemically unstable situation
40.0 %
1 commercial farm with 0 – 20 % seropositive cattle:
Minimal disease or disease-free situation
20.0 %
Fig. 4. 7. Endemic stability to Babesia bigemina recorded on the 5 commercial
farms in the survey during 1999.
Babesia bigemina: 1 commercial farm with more than 61% seropositive cattle:
Endemic stability or a situation approaching endemic stability
1 commercial farms with 21 – 60 % seropositive cattle:
Endemically unstable situation
0 commercial farm with 0 – 20 % seropositive cattle:
Minimal disease or disease-free situation
50.0 %
50.0 %
0.0 %
Fig. 4. 8. Endemic stability to Babesia bigemina recorded on the 2 commercial
farms in the survey during 2000.
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4. 3. Tick collection results from the survey area during 1999 and 2000.
The results of the tick collections are summarized in Tables 4.27-4. 30. A total of 25,042
Boophilus ticks were collected in the study area from 29 dip tanks and 5 commercial
farms. Of these 1,530 (6.1 %) were Boophilus decoloratus and 23,512 (93.9 %)
Boophilus microplus.
Thirteen percent of the Boophilus microplus ticks and 9.2 % of the Boophilus
decoloratus ticks were males.
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4. 3. 1. Tick collection results from the communal dip tanks during 1999 and 2000.
The results of the tick collections are given in Tables 4. 27 and 4.28.
Table 4. 27. Boophilus ticks collected from cattle at dip tanks during 1999.
Dip tank
May 1999
B. dec.
B. micro.
November 1999
December 1999
B. dec.
B. dec.
B. micro.
B. dec.
B. micro.
554
73
579
Thononda
73
25
Dzondo
0
534
0
534
Guyuni
0
448
0
448
Sendedza
133
6
170
410
Luvhanga
4
517
4
517
Muledzhi
0
29
0
625
Malavuwe
0
570
0
570
Makwarani
0
524
0
524
Lamvi
0
286
0
954
Tshaulu
0
496
0
496
0
259
247
5916
Davhana
Total
210
3435
B. dec. = Boophilus decoloratus
0
Total
B. micro.
37
0
0
404
596
668
0
259
0
1523
37
958
B. micro. = Boophilus microplus
In 1999 Boophilus microplus was found together with Boophilus decoloratus at 3 of the
11 dip tanks, Boophilus microplus only was found at 8 dip tanks and at none of the dip
tanks was Boophilus decoloratus found on its own. Of the 6,163 Boophilus ticks
collected at the dip tanks in 1999, 247 (4 %) were Boophilus decoloratus whilst 5,916
(96 %) were Boophilus microplus.
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Table 4. 28. Boophilus ticks collected from cattle at dip tanks during 2000.
Dip tank name
May/ June 2000
October 2000
B. dec.
B. dec.
B. micro.
B. micro.
December 2000
B. dec.
B. micro.
Total
B. dec.
B. micro.
Thononda
0
1691
0
1691
Mahagala
0
901
0
901
Matshena
0
0
0
0
Phiphidi
0
1224
0
1224
Shakadza
0
474
0
474
Fesekraal 1
0
14
0
14
Matatani
0
1256
0
1256
Tshiendeulu
39
941
39
941
Khakhu
0
1413
0
1413
Murangoni
0
1491
0
1491
Gondeni
0
905
0
905
Savhani
0
916
0
916
Tshikotoni
0
543
0
543
Mphephu
4
383
4
383
Keerweerder
35
1
35
1
Masetoni
0
251
0
251
Fripp
0
20
0
20
Maunguwi
0
1562
0
1562
Sambandou
0
714
0
714
Makonde Project
0
306
0
306
0
2582
78
15,006
Total
39
11,769
B. dec. = Boophilus decoloratus
39
655
B. micro. = Boophilus microplus
88
University of Pretoria etd – Tonnesen, M (2005)
In 2000 Boophilus microplus was found together with Boophilus decoloratus at 3 of the
20 dip tanks, B. microplus only was found at 16 of the dip tanks, and at 1 of the dip
tanks no Boophilus ticks were found. Boophilus decoloratus was never found on its own
at any of the dip tanks. Of the 15,084 Boophilus ticks collected at the dip tanks in 2000,
only 78 (0.52 %) were Boophilus decoloratus and 15,006 (99.48 %) were Boophilus
microplus.
4. 3. 2. Tick collection results from the commercial farms during 1999 and 2000.
The results of the tick collections are given in Tables 4. 29 and 4. 30.
Table 4. 29. Boophilus ticks collected from cattle on commercial farms during 1999.
September 1999
B. dec.
B. micro.
November 1999
B. dec.
B. micro.
Nooitgedacht
0
17
Zwartrandjes
63
0
45
0
Modderfontein
16
189
36
50
Mara Res. St.
1
0
Naboomkop
9
45
16
42
Total
89
251
97
92
B. dec. = Boophilus decoloratus
December 1999
B. dec.
B. micro.
265
265
0
0
Total
B. dec
B. micro.
0
17
373
0
52
239
1
0
25
87
451
343
B. micro. = Boophilus microplus
In 1999 Boophilus microplus was found together with Boophilus decoloratus on 2 of the
5 farms, Boophilus microplus only was found on 1 farm and Boophilus decoloratus was
found on its own on 2 farms. A total of 794 Boophilus ticks were collected from the
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commercial farms during 1999 and of these were 451 (56.8 %) Boophilus decoloratus
and 343 (43.2 %) were Boophilus microplus.
Table 4. 30. Boophilus ticks collected from cattle on commercial farms during 2000
and 2001.
May/June 2000
Farm name
B. dec.
B. micro.
Zwartrandjes
123
0
Modderfontein
158
715
Mara Res. St.
44
0
Naboomkop
0
1403
325
2118
Total
October 2000 December 2000 February 2001
B. dec. B. micro.
96
B. dec. B. micro.
B. dec. B. micro.
0
5
129
328
96
B. dec. = Boophilus decoloratus
0
5
129
328
0
0
Total
B. dec. B. micro.
219
0
163
844
372
0
0
1403
754
2247
B. micro. = Boophilus microplus
In 2000 Boophilus microplus was found together with Boophilus decoloratus on 1 of the
4 farms, Boophilus microplus only was found on 1 farm whilst Boophilus decoloratus
was found on its own on 2 farms. Of the 3,001 Boophilus ticks collected from the
commercial farms in 2000, 754 were Boophilus decoloratus (25.1 %) and 2,247
(74.9 %) were Boophilus microplus.
90
4. 4. Displacement of Boophilus decoloratus by Boophilus microplus in the survey area.
4. 4. 1. Tick collection results recorded during the displacement process.
The results of the tick collections are given in Table 4. 31.
Table 4. 31. Tick collections obtained by repeatedly sampling farms and/or dip tanks where Boophilus decoloratus and
Boophilus microplus co-existed during the survey.
Dip tank/farm
May 1999
Sept. 1999
B. dec. B. micro.
B. dec. B. micro.
Nov. 1999
Dec. 1999
May/June
2000
Dec. 2000
B. dec. B. micro.
B. dec. B. micro.
B. dec. B. micro.
B. dec. B. micro.
Thononda
73
25
0
554
Sendedza
133
6
37
404
0
1691
Modderfontein
16
189
36
50
158
715
Naboomkop
9
45
16
42
0
1430
B. dec. = Boophilus decoloratus
5
129
B. micro. = Boophilus microplus
91
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4. 4. 2. Ecoclimatic Indices for Boophilus microplus and Boophilus decoloratus
recorded at the communal dip tanks and commercial farms.
Table 4. 32. Ecoclimatic Indices for Boophilus microplus and Boophilus
decoloratus.
Ecoclimatic Index
Dip tank/farm B. microplus B.decoloratus
Fesekraal
0
1
Matshena
0
1
Matatani
0
4
Shakadza
8
22
Lamvi
8
22
Tshikotoni
6
19
Savhani
9
20
Masetoni
4
17
Guyuni
7
20
Sambandou
4
16
Malavuwe
2
16
Mahagala
7
22
Maunguwi
19
27
Makonde
5
18
Tshaulu
6
22
Tshiendeulu
15
21
Khakhu
12
18
Makwarani
16
21
Mphephu
10
21
Thononda
16
21
Sendedza
19
25
Murangoni
18
22
Gondeni
23
29
Phiphidi
20
26
Muledzhi
23
29
Fripp
5
19
Keerweerder
0
3
Luvhanga
4
16
Dzondo
20
27
Mara
0
4
Nooitgedacht
9
20
Naboomkop
5
17
Davhana
2
6
Zwartrandjes
3
13
Modderfontein
4
14
92
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4. 5. Comparison of the Boophilus tick numbers and the serology results obtained
during 1999 and 2000.
The serology results from communal dip tanks and commercial farms were compared
with the Boophilus tick species found at the time of the bleeding. The results are given in
Tables 4. 33-4. 37.
Table 4. 33. Mean seroprevalence of Babesia bovis and Babesia bigemina from those
dip tanks/farms where only Boophilus decoloratus was recorded in 1999.
Zwartrandjes
Mara Res.St.
No. tested
60
60
Total
120
Babesia bovis
No. pos. % pos.
9
15.0%
3
5.0%
12
Mean
10.0%
Babesia bigemina
No. pos.
% pos.
39
65.0%
32
53.3%
71
59.2%
Table 4. 34. Mean seroprevalence of Babesia bovis and Babesia bigemina from those
dip tank/farms where Boophilus decoloratus and Boophilus microplus co-existed in
1999.
Thononda
Sendedza
Luvhanga
Modderfontein
Naboomkop
Total
No. tested
60
60
60
60
60
300
Babesia bovis
No. pos. % pos.
38
63.3%
26
43.3%
44
73.3%
36
60%
6
10%
150
Mean
50.0%
Babesia bigemina
No. pos.
% pos.
19
31.7%
38
63.3%
39
65%
39
65%
32
53.3%
167
55.7%
93
University of Pretoria etd – Tonnesen, M (2005)
Table 4. 35. Mean seroprevalence of Babesia bovis and Babesia bigemina from
those dip tank/farms where only Boophilus microplus was recorded in 1999.
Dzondo
Guyuni
Muledzhi
Malavuwe
Makwarani
Lamvi
Tshaulu
Nooitgedacht
No. tested
60
60
60
60
60
60
60
60
Total
480
Babesia bovis
No. pos. % pos.
43
71.7%
40
66.7%
50
83.3%
30
50.0%
42
70.0%
51
85.0%
33
55.0%
3
5.0%
292
Mean
60.8%
Babesia bigemina
No. pos.
% pos.
35
58.3%
37
61.7 %
43
71.7 %
37
61.7 %
37
61.7 %
30
50.0 %
42
70.0 %
3
5.0 %
264
55.0%
Table 4. 36. Mean seroprevalence of Babesia bovis and Babesia bigemina from
those dip tanks/farms where Boophilus decoloratus and Boophilus microplus coexisted in 2000.
Tshiendeulu
Mphephu
Keerweerder
Modderfontein
Total
No. tested
60
60
60
60
240
Babesia bovis
No. pos. % pos.
46
76.7%
32
53.3%
0
0.0%
40
66.7%
118
Mean
49.2%
Babesia bigemina
No. pos.
% pos.
30
50.0%
39
65.0%
20
33.3%
18
30.0%
107
44.6%
94
University of Pretoria etd – Tonnesen, M (2005)
Table 4. 37. Mean seroprevalence of Babesia bovis and Babesia bigemina from
those dip tanks/farms where only Boophilus microplus was recorded in 2000.
Mahagala
Phiphidi
Shakadza
Fesekraal
Matatani
Khakhu
Murangoni
Gondeni
Savhani
Tshikotoni
Masetoni
Fripp
Maunguwi
Sambandou
Makonde Proj.
Naboomkop
Total
No. tested
60
41
60
60
60
60
60
60
60
60
60
60
60
60
60
60
941
Babesia bovis
No. pos. % pos.
53
88.3%
29
70.7%
50
83.3%
6
10.0%
36
60.0%
57
95.0%
52
86.7%
47
78.3%
48
80.0%
35
58.3%
47
78.3%
25
41.7%
47
78.3%
49
81.7%
33
55.0%
29
48.3%
643
Mean
68.3%
Babesia bigemina
No. pos.
% pos.
36
60.0%
22
53.7%
42
70.0%
8
13.3%
15
25.0%
55
91.7%
46
76.7%
33
55.0%
27
45.0%
12
20.0%
38
63.3%
39
65.0%
37
61.7%
31
51.7%
21
35.0%
39
65.0%
501
53.2%
95
University of Pretoria etd – Tonnesen, M (2005)
Table 4. 38. Summary of seroprevalence of Babesia bigemina and Babesia bovis
related to vector occurrence at all dip tanks/farms sampled during 1999.
Dip tanks/farms where B.
Dip tanks/farms where
Dip tanks/farms where
decoloratus and B. microplus
only B. microplus was
only B. decoloratus was
were recorded
recorded
recorded
B. bovis
50.0 %
60.8 %
10.0 %
B. bigemina
55.7 %
55.0 %
59.2
Table 4. 39. Summary of seroprevalence of Babesia bigemina and Babesia bovis related
to vector occurrence at all dip tanks/farms sampled during 2000.
Dip tanks/farms where
Dip tanks/farms where
B.decoloratus and
only B. microplus was
B.microplus were recorded
recorded
B. bovis
49.2%
68.3%
B. bigemina
44.6%
53.2%
96
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CHAPTER 5. DISCUSSION
5. 1. Serological findings.
Serological tests are useful tools to assess the degree of exposure of a herd to tick-borne
diseases, and to act as sensitive markers for the presence of certain tick vectors. In the
present survey 2201 blood samples from cattle at 30 communal dip tanks and 5
commercial farms were screened for antibodies to Babesia bovis and Babesia bigemina,
using the IFAT. The results are detailed in Tables 4. 1–4. 26.
5. 1. 1. Interpretation of the IFAT. The IFA test can also detect colostral antibodies,
and the mean extinction point of colostral antibodies to Babesia bigemina is 119 days
(Ross and Löhr, 1970). Antibodies against Babesia bigemina or Babesia bovis in calves
older than four months are considered to be a sign of Babesia infection (Mahoney et al.,
1981). Antibodies are detected by IFAT 2-4 weeks after infection (Anon., 1984) and are
detectable for several years (Mahoney et al., 1973; Mahoney et al., 1979a; Mahoney et
al., 1981). Chronically infected animals may have low titres and the sera could be
classified as negative (Anon., 1984). Drug sterilization of Babesia bigemina and
Babesia bovis in infected animals is followed by a rapid loss of reactivity in the test,
without loss of immunity (Callow et al., 1974a; 1974b; Callow et al., 1993). The
interpretation of serological reactions in older cattle therefore requires some caution,
and should be guided by careful characterization of the test employed, e.g. a negative
test in a previously infected animal may not necessarily indicate the loss of infection
and immunity (Callow et al., 1974b; Mahoney, 1974; Anon., 1984). Todorovic and
Long (1976) found positive IFAT reactions in subclinical infections, but the prevalence
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University of Pretoria etd – Tonnesen, M (2005)
and incidence might be under-estimated in serological surveys of babesiosis (Anon,
1984).
5. 1. 2. Serological cross-reactions. Although the IFAT is widely used for detection of
antibodies to Babesia bovis and Babesia bigemina, serological cross-reactions may
occur. Shortly after Babesia bigemina infection, false positive reactions to Babesia
bovis can occur, and these may last for several weeks (Smith et al., 1980; Bessenger and
Schoeman, 1983). A positive Babesia bovis test can give positive titres to Babesia
bigemina (Smith et al., 1980; Bessenger and Schoeman, 1983). Babesia occultans and
several other Babesia species can give cross-reactions during acute disease or shortly
afterwards (Bessenger and Schoeman, 1983; Papadopoulos et al., 1996; De Waal,
personal communication, 2000). High titres are sometimes obtained against the
homologous antigen while lower titres are obtained against the heterologous antigen
(Smith et al., 1980). This might be due to mixed infections or to cross-reactions, and the
use of IFAT is not always satisfactory for diagnosing infections in areas where both
Babesia bovis and Babesia bigemina are present.
In the field mixed infections are common and cross-reactions tend to increase when the
cattle are infected with both Babesia species (Papadopoulos et al., 1996). However,
Tjornehoj et al. (1996) found no evidence of cross-reaction between the two species at a
dilution of 1/90. Zwart and Brocklesby (1979) and Smith et al. (1980) concluded that
the test is sufficiently specific to determine the prevalence of Babesia bovis and Babesia
bigemina where the species coexist. The IFAT is regarded as a reliable test for studying
Babesia bovis (Johnston et al., 1973; OIE, 1996), but might be lacking in sensitivity and
specificity for Babesia bigemina (Callow, 1979). Low titres of Babesia bovis antibodies
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in areas where the parasite does not occur can be explained by these cross-reactions
(Bessenger and Schoeman, 1983). Todorovic and Long (1976) reported only negative
samples in cattle from known Babesia-free areas and concluded that the IFAT was
reliable when indicating absence of infection.
5. 1. 3. Serological findings from cattle sampled at communal dip tanks during
1999 and 2000.
•
Babesia bovis. Babesia bovis was widespread in the cattle population in
the survey area, with positive reactors in 97 % of the herds and an overall
seroprevalence of 63 % over the two years. There was a non-significant
(p=0.4866) increase in seroprevalence in the older cattle from 1999 to
2000. The younger cattle showed a non-significant decrease in Babesia
bovis from 1999 to 2000 (p=0.2179). For all the cattle in the survey there
was a non-significant decrease in seroprevalence from 1999 to 2000
(p=0.7078). Many of the herds in the drier areas were endemically
unstable to Babesia bovis, and clinical cases of Asiatic redwater were
common (Loock, 2000, personal communication, Fig. 1. 1). The lower
transmission rate in the younger animals in 2000 may have contributed to
this instability.
Virtually all (10/11) of the dip tanks sampled in 1999 were located in the Sour Lowveld
Bushveld (Low and Rebelo, 1996), but only half (10/20) of those sampled in 2000 were
located in this veld type. When selecting dip tanks for sampling in 2000, an effort was
made to include dip tanks in the drier parts of the survey area in order to determine the
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limit of Babesia bovis occurrence. This may have skewed the serology results in 2000,
and to eliminate this confounding factor, dip tanks with similar rainfall, minimum and
maximum temperatures and vegetation were compared in 1999 and 2000.
There was a significant (p=0.0001) increase in the seroprevalence for Babesia bovis
from 1999 to 2000 in cattle inhabiting Sour Lowveld Bushveld. When the
seroprevalence of Babesia bovis in cattle in Sour Lowveld Bushveld was compared with
that of cattle at all the dip tanks, the overall slight decrease seen in the dip tank herds
from 1999 to 2000 seemed to be due to the selection of dip tanks, rather than to a real
decrease in transmission of the blood parasite.
Boophilus microplus has a patchy distribution in South Africa and serological surveys
have indicated that Babesia bovis is unevenly distributed in the country. Few of these
surveys have been conducted in communal farming areas. Tice et al. (1998) tested
young cattle from four communally grazed areas in North West Province and
Mpumalanga, and found that the prevalence of Babesia bovis varied greatly from year
to year and from area to area. None of the four areas were endemically stable for
Babesia bovis, yet no outbreaks of clinical disease were recorded (Tice et al., 1998).
Dreyer et al. (1998c) reported that the seroprevalence of Babesia bovis was close to
20 % in the Free State Province, and concluded that these findings were due to factors
other than tick transmission. Boophilus microplus had never been reported in the Free
State and there had been no outbreaks of disease due to Babesia bovis.
Extensive surveys have been made of the distribution of Babesia bovis in communal
farming areas in other southern African countries (Norval et al., 1983; Bryant and
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University of Pretoria etd – Tonnesen, M (2005)
Norval, 1985; Jagger et al., 1985; Jongejan et al., 1988; Katsande et al., 1999; Smeenk
et al., 2000; Backx, personal communication, 2001). In some areas in Zimbabwe
Babesia bovis was present at 50 to 100 % of the dip tanks. Most herds were endemically
unstable but the trend seemed to favour greater stability in the areas where the blood
parasite was common (Norval et al., 1983; Bryant and Norval, 1985; Katsande et al.,
1999; Smeenk et al., 2000).
Babesia bovis was present throughout Mozambique and the herds appeared to be
endemically stable (Backx, personal communication, 2001). Surveys indicated that
Babesia bovis was common in cattle in many of the areas sampled in Swaziland (Jagger
et al., 1985) and Zambia (Jongejan et al., 1988); 50-80 % of the herds contained
seropositive cattle, but they were mostly in an unstable or minimal-disease situation.
In the present survey Babesia bovis was more widespread and the seroprevalence was
higher in the communal farming areas than was reported by many of the previous
studies. The situation resembled that found in Zimbabwe, where Babesia bovis was
common among the cattle at the dip tanks where Boophilus microplus was present and
where there was minimal tick control.
•
Babesia bigemina. The present study indicated that Babesia bigemina was
widespread in the communal farming area with seropositive reactors in all
of the herds surveyed. The reduction in the Babesia bigemina
seroprevalence from 1999 (56.1 %) to 2000 (49.3 %) was significant
(p=0.006); this was attributed to a decrease in the prevalence in the young
animals (p=0.0002). The seroprevalence of Babesia bigemina was lower
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University of Pretoria etd – Tonnesen, M (2005)
than in many earlier studies, and clinical outbreaks of bovine babesiosis due
to Babesia bigemina were reported in the study area (Loock, 2000, personal
communication, Fig. 1. 1).
Boophilus decoloratus is widespread in South Africa (Walker, 1991) and
previous serological surveys undertaken in communal farming areas in South
Africa have shown that Babesia bigemina infections were more common
than Babesia bovis infections. Tice et al. (1998) found positive reactors in all
of the communal areas tested, and even though the prevalence was low, there
were no reports of clinical disease. Dreyer et al. (1998c) recorded 60-70 %
seroprevalence of Babesia bigemina in two communal grazing areas in the
Free State Province, without any clinical cases being reported.
In surveys in other southern African countries it was found that Babesia
bigemina was widespread in the communal grazing areas. In Zimbabwe
Babesia bigemina was present in nearly all of the herds sampled, and the
herds were only endemically unstable if they were dipped too frequently
(Norval et al., 1983; Bryant and Norval, 1985; Katsande et al., 1999;
Smeenk et al., 2000). Similar results were reported from Swaziland (Jagger
et al., 1985) and Zambia (Jongejan et al., 1988), where few clinical cases
were reported.
There was an overall non-significant (p=0.1941) decrease in seroprevalence of Babesia
bigemina from 1999 to 2000 at dip tanks located in Sour Lowveld Bushveld. The
decrease in the young cattle was significant (p=0.0287), however, which confirms the
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finding of an overall lower transmission rate in the young animals at all dip tanks during
2000.
5. 1. 4. Serological findings from cattle sampled on the commercial farms during
1999 and 2000. The sample size for the commercial farms was small. In 1999 five
farms were included in the survey, but three of them were not re-sampled in 2000. Low
seroprevalence of Babesia bovis and Babesia bigemina was found on these farms in
1999. Two of the farmers vaccinated their cattle in 2000 and the third farm, the Mara
Research Station, was not included in 2000 due to a sampling error. The blood sampling
at Mara was done on cattle from one herd only and this herd had grazed in the few
camps that were specifically allotted to the herd. It was felt that the sample was not
representative for all the cattle at the Research Station. The serology results from the
commercial farms in 2000 thus came from only two units.
•
Babesia bovis. In the present study Babesia bovis was widespread in the
commercial farming areas, and the prevalence was higher than reported in
most of the earlier studies. Seropositive cattle were found on all of the farms
during 1999 and 2000, and the seroprevalence increased significantly
(p=0.0001) from 19 % in 1999 to 57.5% in 2000. This could be attributed to
the high infection rates in both old and young animals. The seroprevalence
of Babesia bovis on the commercial farms in 2000 was similar to the
seroprevalences reported by de Vos (1979) on farms where poor tick control
was practised.
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In earlier surveys in southern Africa it was found that Babesia infections in
cattle kept on commercial farms were less widespread and at a lower
seroprevalence than in cattle kept in communal grazing areas (De Vos, 1979;
De Vos and Every, 1981; Gray and de Vos, 1981; Norval et al., 1983; De
Vos and Potgieter, 1983; Smeenk et al., 2000). De Vos (1979) reported great
variation in the seroprevalence of Babesia bovis between farms in South
Africa. The variation was dependent on the presence of the tick vector and
the efficiency of the dipping programme. In areas favourable for Boophilus
microplus, almost all of the commercial herds where poor tick control was
practised had seropositive reactors to Babesia bovis, and these herds were
endemically stable (De Vos, 1979). On other farms where the tick control
was better, the seroprevalence of Babesia bovis was only 10-30 % and the
herds were endemically unstable. Other surveys in South Africa (De Vos and
Every, 1981; Gray and de Vos, 1981; De Vos and Potgieter, 1983) reported
that Babesia bovis was present on less than 40 % of the farms and the
seroprevalence varied between 2-60 %.
Studies conducted in Zimbabwe (Norval et al., 1983; Smeenk et al., 2000)
revealed that Babesia bovis was present on 20-75 % of the commercial
farms, with a seroprevalence of less than 20 % in most herds. Most of the
commercial farms in these studies were endemically unstable for Babesia
bovis.
•
Babesia bigemina. In the present survey all of the commercial farms had
seropositive reactors to Babesia bigemina and the parasite appeared to be
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widespread. The seroprevalence of Babesia bigemina decreased slightly
from 48 % in 1999 to 47.5 % in 2000. These results were in agreement with
those of earlier studies in South Africa (De Vos, 1979; Gray and de Vos,
1981; de Vos and Potgieter, 1983).
Large areas of South Africa are favourable for Boophilus decoloratus, and
Babesia bigemina has been found over large parts of the country, with
seropositive cattle reported from 80-100 % of the commercial farms (De
Vos, 1979; Gray and de Vos, 1981; de Vos and Potgieter, 1983). On farms
with good tick control the seroprevalence in the cattle was low, and these
herds were endemically unstable. On farms where less efficient tick control
was practised, nearly 100 % of the cattle were seropositive, and these herds
were endemically stable to Babesia bigemina.
In Zimbabwe Babesia bigemina was present on only 40-70 % of the
commercial farms sampled, and the seroprevalence was low (Norval et al.,
1983; Smeenk et al., 2000). Most of the farmers practised intensive tick
control with the result that their herds were in an endemically unstable
situation.
Both Babesia bovis and Babesia bigemina were widespread in the commercial herds
sampled in this region of South Africa, but the sample size (n = 5) was too small to
extrapolate the results to other areas. Antibodies to both Babesia bovis and Babesia
bigemina were found in cattle on all of the commercial farms during 1999 and 2000.
The prevalence of Babesia bovis in the present survey was higher than in most of the
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earlier studies in southern Africa (De Vos, 1979; Norval et al., 1983; Gray and de Vos,
1981). The prevalence of Babesia bigemina in herds on the commercial farms was
comparable to earlier results from farms with medium tick control (Norval et al., 1983;
Gray and de Vos, 1981).
The transmission of Babesia bovis and Babesia bigemina occurred readily on both
commercial farms sampled in 2000. The percentage of cattle seropositive to Babesia
bovis increased from 19 % in 1999 to 57.5 % in 2000 (p=0.0001). The increase could be
attributed to the high transmission rate in both old and young animals. The
seroprevalence of Babesia bigemina remained constant. The high transmission rate of
Babesia bovis on the commercial farms coincided with an increase in Boophilus
microplus numbers during the same period.
The unusually high rainfall in 2000 appeared to have had more influence on tick control
and transmission of TBD in the commercial farm herds when compared with the
communally grazed cattle. The commercial farms experienced a substantial increase in
Boophilus microplus numbers during the survey period, and there were losses due to
redwater amongst cattle in the 18-24-month-old group, as well as amongst cattle
introduced from other areas. One can speculate that the frequent rain prevented the
commercial farmers from carrying out their normal tick control programme, thus
enhancing tick survival. During the flooding the commercial farmers had a much wider
choice of grazing areas available for their cattle than the communal farmers, and they
could graze their cattle on higher ground less affected by the rising water. In these areas
the Boophilus microplus larvae would have been able to survive and multiply.
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5. 1. 5. Statistical significance of the serological results from the communal dip
tanks and the commercial farms. In 1999 the seroprevalence of both Babesia
bigemina and Babesia bovis was significantly higher (p=0.0261 and p=0.0001,
respectively) in the communally grazed cattle when compared with that of the cattle on
the commercial farms. In 2000, however, the seroprevalences of the communally grazed
herds and the commercial farm herds showed no significant difference either for
Babesia bovis (p=0.2890) or for Babesia bigemina (p=0.7030) at the end of the season.
The details are found in Table 4. 25.
When all the animals sampled are considered, there was an overall significant increase
(p=0.0001) in seroprevalence of Babesia bovis from 1999 to 2000. The overall
seroprevalence for Babesia bigemina decreased significantly (p=0.0366) from 1999 to
2000. The non-significant (p=0.6804) decline in the older cattle was offset by a
significant decline in the younger animals (p=0.0130). The details are found in Tables
4- 26.
The higher seroprevalence of Babesia bovis compared to Babesia bigemina found at the
communal dip tanks was difficult to explain. One would expect to find a higher
transmission rate and seroprevalence for Babesia bigemina when compared to those of
Babesia bovis, due to the higher infection rate of Babesia bigemina in the Boophilus
ticks (Mahoney, 1969; De Vos, 1979; De Vos and Potgieter, 1983). Several studies
from southern Africa (Norval et al., 1983; Bryant and Norval, 1985; Smeenk et al.,
2000; Spickett, personal communication, 2001) have reported a higher seroprevalence
of Babesia bovis compared to Babesia bigemina where both parasites co-exist.
Tjornehoj et al. (1996) monitored an outbreak of Asiatic redwater in Malawi where,
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within a period of three months, 75 % of previously negative animals had seroconverted
to Babesia bovis, compared to only 36 % to Babesia bigemina.
In the present study the prevalence of Babesia bovis in the communally grazed areas in
1999 was non-significantly higher (p=0.3278) than that of Babesia bigemina (63.3 %
compared to 56.1 %) but in 2000 the difference (62.4 % compared to 49.3 %) was
significant (p=0.0141).
A similar pattern was found on the commercial farms. In 1999 the seroprevalence for
Babesia bovis was low (19 %), probably due to low Boophilus microplus numbers. In
2000, when Boophilus microplus became more numerous, the seroprevalence of
Babesia bovis increased and eventually exceeded that of Babesia bigemina.
The overall seroprevalence of Babesia bovis in all animals in 1999 was not significantly
(p=0.6291) different from that of Babesia bigemina. This may have been as a result of
the low seroprevalence of Babesia bovis on the commercial farms due to low Boophilus
microplus numbers in 1999. In 2000 there was an influx of Boophilus microplus onto
these farms, the transmission of both Babesia species was good and the seroprevalence
of Babesia bovis for all animals in the survey was significantly (p=0.0142) higher than
that of Babesia bigemina.
5. 2. Endemic stability to Babesia bovis and Babesia bigemina.
The concept of endemic stability has been reviewed in Chapter 2. Briefly, Mahoney and
Ross (1972) and Norval et al. (1983) developed different models for bovine babesiosis
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which were based on the serological results from a group of young cattle aged up to 9
months. In the present study the serological data from the whole herd was used as a
basis for any conclusions on endemic stability. The inclusion of the older animals in this
study may have overestimated the number of endemically stable herds, but would give a
more realistic view of the real risk of TBD outbreaks.
5. 2. 1. Endemic stability to Babesia bovis and Babesia bigemina found in the cattle
sampled at the dip tanks during 1999 and 2000.
The results are shown in Fig. 4. 1-4. 4.
•
Babesia bovis. The percentage of communally grazed herds in the study
area which were endemically stable or were approaching stability to
Babesia bovis was close to 60 % and did not change much from 1999 to
2000. Positive cattle to Babesia bovis were found at 100 % of the dip tanks
during 1999 and at 97 % of the dip tanks in 2000. More herds appeared to
be in a minimal disease or disease-free situation in 2000 compared to 1999,
but many of these dip tanks were located in areas that were marginal for the
survival of Boophilus ticks.
•
Babesia bigemina. The percentage of communally grazed herds in this
study, which had reached endemic stability or were approaching endemic
stability to Babesia bigemina was high (60 %) in 1999, but declined to less
than 40 % in 2000. The reasons for the loss of endemic stability to Babesia
bigemina appeared to be due to a lower infection rate in the younger animals
in 2000, as well as unfavourable conditions for Boophilus tick survival.
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Most of the farmers in the communal farming areas had previously had access to a free
government programme where dipping was carried out weekly or fortnightly. From
2000 the farmers had to pay for these services, and dipping became irregular. During
February and March 2000 dipping was impossible in much of the study area, as dip
tanks were flooded or were inaccessible due to the exceptionally high rainfall. Under
these circumstances one would have expected TBD to become a serious problem, but
the exact level of clinical disease was unknown. Few clinical cases of TBD were
reported to the State Veterinarian in 2000, and all these cases came from the
Thohoyandou district, which had the easiest access to the laboratory at Sibasa.
Communication in the survey area was severely hampered for the rest of the year as
farmers were unable to notify the veterinarians if problems were encountered, so the
real extent of losses due to redwater was unknown.
When dip tanks located in Sour Lowveld Bushveld were compared for endemic stability
to Babesia bovis, there was a slight increase in herds that were endemically stable or
were approaching endemic stability (70 % in 1999 to 80 % in 2000). The percentage of
herds that were endemically stable or were approaching endemic stability to Babesia
bigemina decreased from 70 % in 1999 to 30 % in 2000. The trend towards less
endemic stability to Babesia bigemina, which was recorded in the total sample in 2000,
was real and was not affected by location of the dip tank.
Norval et al. (1983) reported that the loss of endemic stability to Babesia bigemina was
more common in areas where Boophilus microplus was well established, and they
suggested that Babesia bigemina may be transferred less efficiently by Boophilus
microplus than by Boophilus decoloratus. The influx of Boophilus microplus into the
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survey area was followed by a decrease in Boophilus decoloratus and this may have
affected the transmission of Babesia bovis and Babesia bigemina. In the present study
fewer communally grazed herds had reached endemic stability for Babesia bigemina
when compared with Babesia bovis, and this may have occurred because of the
dominance of the Boophilus microplus population.
5. 2. 2. Endemic stability to Babesia bovis and Babesia bigemina found in the cattle
sampled on the commercial farms during 1999 and 2000.
The results are shown in Fig. 4. 5-4. 8.
•
Babesia bovis. In 1999, 80 % (4/5) of the commercial farm herds
were in a minimal disease or disease-free situation. In 2000, 1 of the
2 herds in the survey was approaching endemic stability and the
other was endemically unstable. One of the main reasons for the shift
in endemic stability status was the increase in the Boophilus
microplus population on the commercial farms, and this was
followed by increased transmission of Babesia bovis. Both
commercial herds, which were bled twice during the survey period,
moved towards greater endemic stability to Babesia bovis.
•
Babesia bigemina. In 1999, 2 of 5 of the herds were endemically
stable or approaching endemic stability to Babesia bigemina, 2 herds
were endemically unstable and 1 herd was disease-free. In 2000, 1 of
2 herds was approaching endemic stability whilst 1 herd was
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unstable. None of the herds were in a minimal disease situation in
2000.
Although the number of commercial farms included in the survey was small, some
trends could be seen. Transmission of Babesia bovis increased significantly in 2000,
while transmission of Babesia bigemina remained constant during the survey period.
Both factors were probably due, directly or indirectly, to the increase in Boophilus
microplus numbers.
5. 2. 3. Endemic stability to Babesia bovis and Babesia bigemina at the dip tanks
compared with endemic stability on the commercial farms.
•
Babesia bovis. In 1999, over 60 % of the communally grazed herds had
reached endemic stability to Babesia bovis, compared with none of the
commercial farm herds. None of the communal herds was disease-free or in
a minimal disease situation, but 80 % of the commercial farm herds were in
this group in 1999. During 2000, the communally grazed herds in the survey
area shifted slightly towards instability to Babesia bovis but the two
commercial farms moved towards greater stability. The difference between
the two farming systems had almost disappeared.
•
Babesia bigemina. In 1999, over 60 % of the communally grazed herds had
reached endemic stability to Babesia bigemina, compared with 40 % of the
commercial farm herds. In 1999, none of the communally grazed herds were
disease-free or in a minimal disease situation, but 20 % of the commercial
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farm herds were in this group. During 2000, the communally grazed herds
shifted towards instability with less than 40 % approaching stability and
60 % being endemically unstable or in a minimal disease situation. The
commercial farm herds, however, moved towards endemic stability. The
change with Babesia bigemina on the commercial farms was not as dramatic
as with Babesia Boris, and little difference could be detected between the
two farming systems. The two commercial herds in this survey had reached
the same level of endemic stability as the communally grazed herds.
5. 2. 4. Correlation between the endemic stability to Babesia bovis and Babesia
bigemina at dip tanks/farms and the presence of specific Boophilus species. In
1999, 60 % of the dip tank/farm herds where only Boophilus microplus was recorded
had reached endemic stability or were approaching endemic stability for both Babesia
bovis and Babesia bigemina. In 2000, 60 % of these dip tank/farm herds had reached
endemic stability or were approaching stability for Babesia bovis, whilst only 45 % had
reached endemic stability or were approaching stability for Babesia bigemina.
Although the tick collection method was not standardised, it appeared that there were
more ticks present on the cattle in 2000 than in 1999. The number of Boophilus ticks
that were collected at the dip tanks/farms doubled from 1999 to 2000 and virtually all
were Boophilus microplus.
In the present study there endemic stability to Babesia bigemina appeared to decline
when only Boophilus microplus was collected at the dip tanks/farms. These findings
support those of Norval et al. (1983), who reported less endemic stability for Babesia
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bigemina when Boophilus microplus was well established. They suggested that Babesia
bigemina was transmitted less efficiently by Boophilus microplus than by Boophilus
decoloratus.
5. 3. Tick collection in the survey area.
5. 3. 1. General discussion of the tick results. The climate in the survey area was well
suited for both Boophilus species, but whilst Boophilus decoloratus was endemic in the
region (Theiler, 1949; Walker 1991), Boophilus microplus had never been recorded
there (Theiler, 1962; De Vos, 1979; Baker et al., 1989; Walker, 1991).
At the start of the survey there was a lack of information on the distribution of the two
Boophilus species in Venda and Soutpansberg, and selected criteria (Chapter 3. 2. 1)
were used to decide which communally grazed areas and commercial farms should be
included in the survey.
It would appear that the spread of Boophilus microplus in the study area was rapid
(Loock, 1999, personal communication). The first cattle losses due to Babesia bovis
were reported as early as 1984, and outbreaks of Asiatic redwater have since escalated
(Loock, 1999, personal communication). The losses were especially heavy in the
communally farmed areas where the exact mortality details were often not known due to
under-reporting by the farmers, but in certain areas the communal farmers lost nearly
half their cattle (Loock, 1999, personal communication; Tshisamphiri, 2000, personal
communication). Initially the cattle in the study area were fully susceptible to Babesia
bovis, and the disease outbreaks appeared to be similar to those reported from
Zimbabwe, where the small-scale farmers also suffered heavy losses after the
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breakdown of dipping and the concomitant influx of Boophilus microplus (Norval,
1982; Norval et al., 1992a).
Some of the commercial farmers had also lost cattle due to Babesia bovis, probably due
to acaricide resistance or a breakdown in dipping routines, and some of them had then
vaccinated their cattle to reduce further losses (Ahrens, 1999, personal communication).
In 1999 Boophilus microplus was already dominant in the communally farmed area.
Low numbers of Boophilus decoloratus were collected even at dip tanks far north and
west in the study area during 2000.
5. 3. 2. Reasons for the variation in tick numbers in the study area. There were large
variations in the number of ticks found on both communally grazed and commercial
cattle, and the following reasons may explain these variations:
•
Some dip tanks/farms maintained a strict dipping schedule throughout
the study period.
•
Some dip tanks/farms were located in areas that were too dry for large
populations of Boophilus ticks to survive.
•
At some of the dip tanks/farms the cattle had been dipped a few days
prior to sampling, and in these cases an effort was made to go back to
these locations for a second tick collection at a later stage.
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•
At some of the dip tanks/farms where both Boophilus decoloratus and
Boophilus microplus were present, the tick numbers may have been low
due to reproductive interference (Spickett and Malan, 1978; Norval and
Sutherst, 1986).
The number of ticks collected from cattle at each dip tank/farm also varied according to
the number of collectors involved, the number of days that had elapsed since the last
dipping, as well as the location of the dip tank/farm. As many ticks as possible were
collected from each dip tank/farm and an attempt was made to collect at least 400 ticks
at each location. If few ticks were collected at the first sampling, the area was resampled in order to get more information on which Boophilus species were present. At
certain dip tanks/farms small numbers of ticks were consistently collected, due either to
harsh climatic conditions or to strict dipping regimens, and only one sampling was
possible at many of these dip tanks. The inconsistency of the sampling procedure must
therefore be taken into consideration before a possible association between the relative
abundance of Boophilus ticks and the seroprevalence of Babesia bovis and Babesia
bigemina can be concluded.
During the first part of the survey an attempt was made to collect Boophilus ticks from
selected body sites on 6 animals at each dip tank/farm. This practice was soon
discontinued, however, as there were few ticks on the cattle in certain regions of the
survey area. As one of the main objectives of the study was to assess the proportion of
Boophilus microplus in relation to Boophilus decoloratus, it was felt that sampling
specific predilection sites of attachment could be over-ridden.
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5. 3. 3. Tick collection from cattle at the dip tanks. Boophilus species were the most
common ticks on cattle at the dip tanks and were common on communally grazed cattle.
This finding is in line with other surveys on communally grazed land where intensive
dipping programmes had been practised for a number of years (Norval, 1978, 1979).
High stocking rates and limited pasture made ideal conditions for Boohpilus larval
survival and host finding (Norval, 1978; 1979; Solorio-Rivera et al., 1999), and high
Boophilus tick numbers were observed on the cattle at most of the dip tanks during this
survey. Overgrazing on communally grazed land removes the ground cover, and the
larvae and nymphs of 2- and 3-host tick species are not able to develop. These
overgrazed pastures are, however, ideal for the survival of Boophilus larvae (Rechav,
1982). Boophilus ticks increase substantially under these circumstances (Norval, 1978;
1979) and when intensive dipping is discontinued, these ticks are the first to appear in
large numbers. Dipping had been carried out intermittently at most of the dip tanks in
Venda and as a consequence the Boophilus numbers were high. After a period of low
tick numbers in February - April 2000 due to flooding, the numbers soon increased
again (Tshisamphiri, 2000, personal communication) when the combined effects of
government dipping policy and the ruined dip tanks became effective. At nearly 80 % of
the dip tanks (n = 30) at least 400 Boophilus ticks were collected during both 1999 and
2000.
During 1999 Boophilus microplus was already the dominant Boophilus species in the
area and was collected from cattle at all (100 %) of the communal dip tanks, whilst
Boophilus decoloratus was found at only 30 % of the dip tanks. At these dip tanks
Boophilus decoloratus comprised 23 % of the total Boophilus count. When selecting the
dip tanks for sampling in 2000, an effort was made to go as far north and west in the
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survey area as possible in order to find areas where Boophilus microplus had not yet
spread. Despite this, Boophilus microplus was found at 95 % of the dip tanks and
Boophilus decoloratus at only 16 % of the dip tanks. At these dip tanks Boophilus
decoloratus comprised 14.7 % of the total Boophilus count.
Of the 6163 Boophilus ticks collected at the dip tanks during 1999, 4 % were Boophilus
decoloratus. During 2000 only 1 % of the 15,084 Boophilus ticks collected were
Boophilus decoloratus.
This survey showed that both Boophilus species were widespread in the communal
grazing areas covered, and that Boophilus microplus was the dominant Boophilus
species at all of the communal dip tanks sampled. Norval et al. (1983) reported finding
Boophilus decoloratus from all climatic zones in Zimbabwe, and this tick was collected
from 58 % of the communal grazing areas whilst Boophilus microplus was collected
from 26 % of these areas.
5. 3. 4. Tick collections from cattle on the commercial farms. In general the cattle on
commercial farms in the survey area carried fewer Boophilus ticks than cattle on
communally grazed land. Pasture management and lower stocking rates on the
commercial farms prevented overgrazing, and 2- and 3-host tick species were more
common on these farms than Boophilus species (Norval, 1978, 1979). Rotation of
pastures was a common practice on the commercial farms, but this practice was not
feasible on the communally grazed land. Pasture spelling can reduce tick numbers
drastically (Johnston et al., 1981; Bigalke et al., 1976).
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Tick numbers were also low as a result of the harsh climatic conditions (Mara Research
Station) or frequent dipping (Nooitgedacht Farm and Zwartrandjes Farm). The two most
westerly farms sampled were the ones where only Boophilus decoloratus was found. At
Modderfontein Farm and Naboomkop Farm both Boophilus species were found during
1999 and the tick numbers may initially have been low due to frequent dipping and
reproductive interference (Spickett and Malan, 1978; Sutherst, 1987a). This changed in
2000 when Boophilus microplus became the dominant tick on these farms and
Boophilus decoloratus almost disappeared. On both farms the total Boophilus numbers
collected increased substantially as Boophilus microplus displaced Boophilus
decoloratus partially or totally. This change on the commercial farms was reflected in
the displacement observed in the communally grazed areas.
Most of the commercial farms had strict dipping routines that were applied to new cattle
on arrival, whilst introductions into communal herds occurred without such precautions.
The spread of Boophilus microplus into new areas is associated with cattle movements
as this is a one-host tick that seldom feeds on hosts other than cattle (Sutherst and
Comins, 1979). One can speculate that the spread of Boophilus microplus to
commercial farms may have occurred after a breakdown of fences, which resulted in
communally grazed cattle straying onto commercial farms. Occasional flooding may
also have contributed to this spread (Callow et al., 1976a).
A total of 3795 Boophilus ticks were collected from the commercial farms during the
survey. During 1999 Boophilus decoloratus was the dominant Boophilus tick on the
commercial farms and was collected from cattle at 4 (80 %) of the 5 farms, whilst
Boophilus microplus was found on 3 (60 %) of the farms. Of the 794 Boophilus ticks
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collected during 1999, 57 % were Boophilus decoloratus and 43 % were Boophilus
microplus. During 2000 Boophilus microplus became the dominant Boophilus species
on the four commercial farms surveyed: 75 % of the 3001 Boophilus ticks collected
were Boophilus microplus and only 25 % were Boophilus decoloratus.
Norval et al. (1983) reported Boophilus decoloratus from 9 % of the commercial farms
sampled in Zimbabwe, while Boophilus microplus was collected from only 3 % of these
localities. These figures are much lower than the findings in this survey and possibly
reflect a change in attitude to dipping amongst the commercial farmers in the study area.
In 1999 only one of the commercial farmers attempted to keep cattle tick-free, whereas
the others all tolerated a certain number of ticks on the cattle.
5. 3. 5. Boophilus tick collections from the communal dip tanks compared with
those from the commercial farms. Boophilus microplus was found in larger numbers
at the communal dip tanks than on the commercial farms. On average, more than four
times as many Boophilus ticks were collected from each dip tank compared with each
commercial farm in 1999. During 2000, more Boophilus were collected from the
commercial farms than during 1999, but more than half of this total came from only one
farm, namely Naboomkop. On this farm few ticks were collected during 1999 when
both Boophilus species were present, but large numbers of ticks were found on the farm
in 2000 when only Boophilus microplus was present. Few ticks were found on the other
commercial farms. During 2000, the average number of ticks collected at the communal
dip tanks was almost double that from the commercial farms.
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Boophilus decoloratus was never found on its own at any of the dip tanks in the
communally grazed areas, but was present on 40 % of the commercial farms in 1999
and 50 % in 2000. Boophilus microplus was found on its own on 20 % of the
commercial farms in 1999 compared with 73 % of the dip tanks. In 2000 Boophilus
microplus was found on its own on 25 % of the commercial farms, compared with 84 %
of the dip tanks.
5. 4. Displacement of Boophilus decoloratus by Boophilus microplus in the survey
area during 1999/2000.
5. 4. 1. Introduction. The distribution of any tick species is never static and often
changes in response to a range of factors, which include the movement of animals,
changes in local dipping programmes, different resistance to acaricides and drought.
Historically, tick species have been introduced onto new continents (Curnow, 1973b;
Payne and Osorio, 1990), and once established their spread is often rapid (Lawrence and
Norval, 1979; Barré et al., 1987; Walker, 1987; Peter et al., 1998). In some cases the
newly introduced tick species has been able to compete successfully with or even
displace a closely related species (MacLeod and Mwanaumo, 1978; Rechav et al., 1982;
Norval, 1983; Sutherst, 1987a; Berkvens et al., 1998.)
In the early 1900s, the first research reports suggested that Boophilus microplus was
displacing Boophilus decoloratus in the south-eastern Cape (as Boophilus fallax,
Howard, 1908 or as Boophilus annulatus, Dönitz, 1910. Cited by Theiler, 1962). Other
reports from southern Africa later confirmed this displacement (Spickett and Malan,
1978; MacLeod and Mwanaumo, 1978; Mason and Norval, 1980; Baker et al., 1981;
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Norval et al., 1983; Norval and Short, 1984; Norval and Sutherst, 1986; Sutherst,
1987b; Berkvens et al., 1998). The actual process of displacement of Boophilus
decoloratus by Boophilus microplus has never been documented in South Africa. One
of the objectives of the present study was aimed at assessing the relative numbers of
Boophilus microplus in relation to Boophilus decoloratus in the study area and
monitoring the possible displacement of Boophilus decoloratus by Boophilus microplus
in the field.
5. 4. 2. Tick findings in the survey area showing displacement. The Boophilus
decoloratus numbers in the survey area declined from 4 % of the total Boophilus count
in 1999 to 1 % in 2000. Where changes in the tick population at the dip tank/farm could
be followed through several samplings, there was a clear tendency for Boophilus
microplus to displace Boophilus decoloratus.
The two tick species were found to co-exist at 6 communal dip tanks (Thononda,
Sendedza, Luvhanga, Tshiendeulu, Mphephu and Keerweerder) and 2 commercial
farms (Naboomkop and Modderfontein). It was only possible to repeat samplings at a
few of these dip tanks, but on the commercial farms repeated samplings were made.
During 1999 and 2000 Boophilus decoloratus co-existed with Boophilus microplus at
23 % of the dip tanks or farms (n = 35). During the study Boophilus decoloratus
appeared to have been completely displaced by Boophilus microplus at Thononda dip
tank and Naboomkop Farm and partially displaced at Sendedza dip tank and
Modderfontein Farm (Table 4. 31). At Luvhanga, Tshiendeulu and Mphephu dip tanks
the numbers of Boophilus decoloratus were low and at Keerweerder dip tank only one
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Boophilus microplus tick was found out of 36 Boophilus ticks collected and there were
no positive reactors to Babesia bovis.
•
Thononda dip tank. In May 1999, 75 % of the Boophilus ticks collected
were Boophilus decoloratus and 25 % were Boophilus microplus. In
December the same year, all (100 %) were Boophilus microplus. It
appeared that Boophilus decoloratus was no longer present at this dip
tank and the finding was confirmed in May 2000 when all Boophilus
ticks were Boophilus microplus.
•
Sendedza dip tank. In May 1999, 95.7 % of the Boophilus ticks
collected were Boophilus decoloratus and only 4.3 % were Boophilus
microplus. In December 1999, 8.4 % of the ticks were Boophilus
decoloratus and 91.6 % were Boophilus microplus. There was a
tendency at this dip tank towards total displacement of Boophilus
decoloratus by Boophilus microplus. The dip tank was destroyed in the
flooding in February 2000 and no more ticks could be collected from this
site.
•
Modderfontein Farm. At the first tick collection from this farm
(September 1999) 7.8 % of the Boophilus ticks collected were Boophilus
decoloratus and 92.2 % were Boophilus microplus. In November 1999,
41.9 % were Boophilus decoloratus and 58.1 % Boophilus microplus. In
May 2000, 18.1 % were Boophilus decoloratus and 81.9 % Boophilus
microplus. In December 2000, only 3.7 % of the ticks were Boophilus
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decoloratus whilst 96.3 % were Boophilus microplus. There was a strong
tendency towards displacement of Boophilus decoloratus by Boophilus
microplus on this farm.
•
Naboomkop Farm. At the first collection from the farm (September
1999) 16.7 % of the Boophilus ticks collected were Boophilus
decoloratus and 83.3 % were Boophilus microplus. In November 1999,
27.6 % of the ticks were Boophilus decoloratus and 72.4 % were
Boophilus microplus. In May 2000, all (100 %) of the ticks were
Boophilus microplus. It appeared that Boophilus decoloratus was no
longer present on the farm and the displacement of Boophilus
decoloratus by Boophilus microplus seemed complete.
The findings in this survey strongly support other surveys where rapid spread of
Boophilus microplus and the displacement of Boophilus decoloratus have been reported
(MacLeod and Mwanaumo, 1978; Mason and Norval, 1980; Baker et al., 1981; Norval
et al., 1983; Berkvens et al., 1998). The hypothesis that Boophilus decoloratus can be
displaced by Boophilus microplus in 1-3 years also seems to have been confirmed
(Sutherst, 1987a).
5. 4. 3. The use of the CLIMEX Ecoclimatic Index (EI) and the CLIMEX maps.
CLIMEX is a computer-software programme designed to model the effects of climate
on the distribution and relative abundance of plants and animals. CLIMEX uses climatic
data together with biological data and known geographic distribution data of species.
The model can be used to predict the spread and potential for development of an
organism into a new geographical area (Sutherst and Maywald, 1985).
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The results are found in Table 4. 32 and the maps are shown in Fig. 5. 1-5. 4.
The communal dip tanks and commercial farms in this survey were scattered over a
large area in Venda and Soutpansberg. All the different locations had different
possibilities for the survival and development of Boophilus ticks and consequently for
the development of endemic stability to Babesia bovis and Babesia bigemina in the
herds.
The higher the EI for a location, the larger the potential for survival of the tick and
therefor for an increase in the population. If the value is lower than about 20 on a scale
of 1-100, then this is an indication that the environment is moderately favourable for the
tick, but the tick species will still be able to survive and multiply. With an EI of less
than 5, the tick numbers on the cattle would be too low to achieve endemic stability to
either Babesia species by tick transmission alone (Sutherst and Maywald, 1985; 1986;
Sutherst, 1987b).
The EIs in the survey area and the matching maps of the possible distribution of
Boophilus decoloratus and Boophilus microplus were computed using 30 years of
climatic data (by courtesy of Prof. R. Schulze, University of Natal).
At some of the dip tanks/farms in the survey area the rainfall was marginal for the
survival of either Boophilus species. There were marked differences in the EIs for
Boophilus decoloratus and Boophilus microplus at all locations in the survey, with
Boophilus decoloratus being the more drought-resistant tick. Some of the dip
tanks/farms had EIs for Boophilus decoloratus of less than 5, and few Boophilus ticks
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were found in these areas. The EI for Boophilus decoloratus was always higher than for
Boophilus microplus; even so, Boophilus decoloratus was collected at only 8 of the 35
dip tanks/farms in the survey. This skewed result clearly shows the displacement of
Boophilus decoloratus by Boophilus microplus.
The mean annual rainfall in the survey area over the past 6 years was almost double that
of the 5 previous years (Data from The South African Weather Bureau). With double
the average rainfall it was possible to show the expected distribution of the two species
during a prolonged wet spell or as a result of a permanent change in the weather pattern
(Fig. 2 and 4).
During a wet cycle conditions for growth and development of Boophilus microplus
were favourable even in areas with normally low EIs, as small amounts of rainfall in the
dry months would considerably reduce the dry stress and make the area more suitable
for Boophilus. At Messina the EI for Boophilus decoloratus is 4 and the EI for
Boophilus microplus is 0 in years with average rainfall. With 25 mm of rain or irrigation
per week during the dry months the EIs can change to 39 and 24, respectively (Sutherst,
personal communication, 2001). The unusually heavy rainfall in the study area over the
past few years may explain why Boophilus microplus had spread so successfully into
the drier part of this region.
In Fig. 5. 2 it is clear that the areas suitable for Boophilus microplus have vastly
expanded. Large numbers of Boophilus microplus were found at dip tanks situated
outside the area where this species would normally be expected to occur. Some of the
communal herds grazed in areas located on the southern slopes of the Soutpansberg
Mountains whilest the dip tank was located on the dry northern slopes (Tshisamphiri,
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personal communication, 2001). In other instances a non-perennial river, a vlei or a
waterhole may constitute a perfect microclimate for the tick (Sutherst and Maywald,
1985).
The climate in many parts of Venda is suitable for Boophilus microplus and the tick will
probably continue to spread and may become permanently established in many of the
different ecological areas adjacent to the dip tanks. To the west of Louis Trichardt as
well and in the Mopani veld north of the Soutpansberg Mountains Boophilus
decoloratus will probably persist, as the climatic conditions are much drier with an EI
for Boophilus microplus close to 0 in years of average or lower rainfall.
Cattle normally develop some resistance to Boophilus microplus after a few months of
exposure (Wagland, 1975; 1978; Sutherst et al., 1979; Sutherst and Utech, 1981). As a
consequence Boophilus microplus loses some advantage over Boophilus decoloratus in
herds which have recently been invaded. As a result of the large fluctuations in annual
rainfall, coupled with the small difference in host adaptations of each species, a seesaw
effect can develop whereby each species sequentially displaces the other. This has been
observed in Zimbabwe and in Swaziland (Norval et al., 1992b; Wedderburn et al.,
1991). These areas can become highly unstable for both Babesia bovis and Babesia
bigemina, as Boophilus numbers never increase enough to maintain the endemic
stability to either parasite.
A pattern of introduction, disappearance and re-introduction of Boophilus microplus can
be expected in some of the regions where the tick was found in substantial numbers
during this survey. Earlier reports have shown that this can happen in South Africa
(Bigalke et al., 1976). A similar occurrence has been described in Zimbabwe where
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Rhipicephalus appendiculatus was introduced at the start of a wet climatic cycle and
disappeared at the end of a dry cycle (Norval and Perry, 1990). In other regions
Boophilus microplus will be able to establish itself permanently, especially in those
areas where the EI is close to or over 20.
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Fig. 5. 1. CLIMEX Ecoclimatic Index map illustrating the predicted distribution of Boophilus
microplus in years with average rainfall.
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Fig. 5. 2. CLIMEX Ecoclimatic Index map illustrating the predicted distribution of Boophilus
microplus in years with double average rainfall.
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Fig. 5. 3. CLIMEX Ecoclimatic Index map illustrated the predicted distribution of Boophilus
decoloratus in years with average rainfall.
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Fig. 5. 4. CLIMEX Ecoclimatic Index map illustrating the predicted distribution of Boophilus
decoloratus in years with double average rainfall.
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5. 5. Possible association between the Babesia seroprevalence and the presence of
Boophilus tick species collected at the communal dip tanks and the commercial farms
during 1999 and 2000.
5. 5. 1. Introduction. During the present survey the seroprevalences of Babesia bovis
and Babesia bigemina in cattle at the communal dip tanks/commercial farms were
compared with the presence or absence of the specific Boophilus tick species. The
seroprevalences in the herds were also compared with the numbers of ticks collected off
the cattle at the time of the bleeding. By monitoring the change in Babesia
seroprevalence, a possible association between seropositive cattle and the ongoing
displacement of Boophilus decoloratus by Boophilus microplus was followed. The
findings in this survey were compared with those of Norval et al. (1983).
5. 5. 2. Possible association between the Boophilus tick species on the cattle and the
mean Babesia bovis seroprevalence.
The results were presented in Tables 4. 23-4. 27
During 1999, the mean seroprevalence of Babesia bovis was 10 % at the dip tanks/farms
where Boophilus decoloratus was the only Boophilus tick recorded. At the dip
tanks/farms where both Boophilus species were present, the mean seroprevalence of
Babesia bovis was 50 %, compared with 60.8 % in herds where only Boophilus
microplus occurred. The latter difference was significant (p=0.0001).
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In 2000, where both Boophilus species were present at the dip tanks/farms, the mean
seroprevalence for Babesia bovis was 49.2 %, compared with 68.3 % where only
Boophilus microplus was present. The difference was significant (p=0.0001).
This increase in the mean seroprevalence of Babesia bovis was to be expected, as high
tick numbers at those dip tanks/farms where only Boophilus microplus was present
would have ensured effective transmission of Babesia bovis. This was supported by the
fact that many of the herds at these dip tanks/farms had reached or were approaching
endemic stability. The strong correlation between the presence of Boophilus microplus
and Babesia bovis confirms that Boophilus microplus is the main and probably the only
vector of Babesia bovis in South Africa (Potgieter, 1977; Norval et al., 1983).
When Boophilus microplus is introduced, the prevalence of Babesia bovis in a herd
would be expected to rise. The high Babesia bovis prevalence found in most herds in
the survey was probably associated with a longstanding infection with Babesia bovis,
and the veterinary records indicated that Babesia bovis had been in the area for the past
15 years. The fact that Boophilus decoloratus was still present and had not been totally
replaced indicated that the infection at the dip tank/farm was recent and a low
seroprevalence of Babesia bovis can be expected.
5. 5. 2. 1. Factors affecting the Babesia bovis seroprevalence during the survey.
Small numbers of positive reactors to Babesia bovis were detected in the absence of
Boophilus microplus at some of the dip tanks/farms. As Boophilus microplus is the only
known vector of Babesia bovis in this part of Africa (Potgieter, 1977; Norval et al.,
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1983), other possible explanations for these positive findings needed to be considered.
These include:
•
Seropositive cattle may have been brought in from the outside as a
cultural exchange (lobola) or as replacement cattle (Norval et al., 1983).
In the northern part of Venda cattle may have been smuggled across the
border from Zimbabwe (Tshisamphiri, personal communication, 2000).
•
Boophilus microplus may have been present at the dip tanks/farms in
small numbers without being detected. (Norval et al., 1983). This
would give a low transmission rate for Babesia bovis and a minimaldisease situation would develop. Dreyer et al., (1998c) recorded
seropositive reactors to Babesia bovis in 20 % of the cattle without
actually finding Boophilus microplus in a sample of 230,000 Boophilus
ticks. It is possible that small numbers of Boophilus microplus may
have been overlooked at some of the dip tanks/farms, as the tick was
not expected to be present in that area (Dreyer et al., 1998c). In the
present
study,
the
numbers
of
ticks
collected
at
the
dip
tanks/commercial farms where only Boophilus decoloratus was found
were very low, so the possibility of Boophilus microplus being present
here could not be excluded.
•
The IFAT may have given false positive reactions. Shortly after
infection with Babesia bigemina false positive reactions to Babesia
bovis are seen (Smith et al., 1980; Bessenger and Schoeman, 1983), and
the low mean seroprevalence of Babesia bovis in areas where the
parasite does not normally occur may be explained by these cross-
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reactions (Bessenger and Schoeman, 1983; Papadopoulos et al., 1996).
Various authors, however, have concluded that the test is sufficiently
specific to determine the prevalence of Babesia bovis and Babesia
bigemina where the species coexist (Zwart and Brocklesby, 1979; Smith
et al., 1980; Tjornehoj et al., 1996).
5. 5. 3. Possible association between the Boophilus tick species on cattle and the
mean Babesia bigemina seroprevalence.
The results were presented in Tables 4. 23-4. 27
During 1999, the seroprevalence of Babesia bigemina was 59.2 % when only Boophilus
decoloratus was recorded at the dip tank/farms. Seroprevalence was 55.7 % where both
Boophilus species were present and 55.0 % where only Boophilus microplus was
collected; these differences were not significant (p=0.7125).
During 2000 the seroprevalence to Babesia bigemina was 44.6 % where both Boophilus
species were present and 53.2 % where only Boophilus microplus was found; the
difference was significant (p=0.0166).
The composition of the Boophilus population at the communal dip tanks/farm herds
where both Boophilus species were present changed from 1999 to 2000. Few Boophilus
ticks were found on the cattle at the 5 dip tanks/farms included in this group in 1999 and
23 % of these were Boophilus decoloratus. In 2000 there were only 4 dip tanks/farms in
the group where both Boophilus species were found, and although the mean number of
collected Boophilus ticks more than doubled, only 10.4 % were Boophilus decoloratus.
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Only small numbers of Boophilus decoloratus were present in the total tick sample
during 2000. The low transmission rate in the young animals that year, together with the
few Boophilus decoloratus ticks collected, may explain why the transmission of
Babesia bigemina in the group with both Boophilus species present was initially low
(44.6 %) when compared to the transmission in the similar group during 1999 (55.7 %).
The average Boophilus numbers collected from cattle at each dip tank/farm increased in
2000, and it is possible that the relatively high seroprevalence of Babesia bigemina at
dip tanks/farms where Boophilus microplus was dominant was a result of the general
increase in Boophilus numbers. In 2000 the seroprevalence of Babesia bigemina in the
group of dip tanks/farms with both Boophilus species present (44.6 %) changed to
53.2 % where only Boophilus microplus present. The seroprevalence of Babesia
bigemina at dip tanks/farms with only Boophilus microplus present in 2000 was still
lower than in the similar group (55 %) the previous year.
The increasing Boophilus microplus numbers at the dip tanks/farms and the low
transmission rate of Babesia bigemina may be the underlying reason for the low
seroprevalence of Babesia bigemina in 2000. The number of dip tanks/farms where both
Boophilus species were found was too small to draw any conclusions.
No significant association was found between the presence of Boophilus decoloratus
and the seroprevalence of Babesia bigemina. During 1999 the seroprevalence of
Babesia bigemina decreased as Boophilus decoloratus was displaced by Boophilus
microplus, but during 2000 the seroprevalence of Babesia bigemina increased.
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Because of the loss of endemic stability in the areas where Boophilus microplus was
dominant, Norval et al. (1983) suggested that Babesia bigemina was transmitted less
efficiently by Boophilus microplus than by Boophilus decoloratus. It was not possible to
confirm this hypothesis in this project. There was, however, a sharp decline in endemic
stability to Babesia bigemina in areas dominated by Boophilus microplus in the present
study. More research is needed on the transmission of Babesia bigemina by the
Boophilus species in Africa.
5. 5. 4. Possible association between the seroprevalence of Babesia bovis and
Babesia bigemina and the presence of Boophilus ticks at the dip tanks/farms. At dip
tanks/farms where both Boophilus species were present, there was no significant
difference in the mean seroprevalence for Babesia bigemina and Babesia bovis either in
1999 or in 2000. During both these years the sample size was small, 5 dip tanks/farms
in 1999 and 4 dip tanks/farms in 2000.
There was a non-significant (p=0.5781) difference in the seroprevalences of Babesia
bigemina and Babesia bovis collected at the 8 dip tanks/farms with only Boophilus
microplus present in 1999, with the seroprevalence of Babesia bovis being higher than
that of Babesia bigemina. This trend was confirmed in 2000 with a significant
difference (p=0.0112) between the seroprevalences of the two Babesia species at the dip
tanks/farms where only Boophilus microplus was present. When all 24 dip tanks/farms
with only Boophilus microplus present during both 1999 and 2000 were compared, the
seroprevalence of Babesia bovis was significantly higher than that of Babesia bigemina
(p=0.0065). When all 22 dip tanks where only Boophilus microplus was present during
both 1999 and 2000 were compared, the difference in seroprevalence of Babesia bovis
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and Babesia bigemina was even more significant (p=0.0028). The results are in Tables
4. 24-4. 4.27
5. 5. 5. Possible association between the relative abundance of Boophilus ticks at
the dip tanks/farms compared with the seroprevalence to Babesia bovis and
Babesia bigemina. In areas which were marginal for tick survival, tick numbers were
low and this resulted in a low transmission rate for both Babesia species. In order for
100 % transmission to occur during the first nine months of their lives exotic cattle need
to be bitten by at least 20 and indigenous breeds by at least 40 ticks a day, respectively
(Mahoney, 1979).
When the dip tanks/farms with similar Boophilus tick numbers were grouped according
to high or low mean tick counts, the low tick counts generally coincided with the low
seroprevalence for both Babesia bovis and Babesia bigemina. If the mean
seroprevalence of Babesia bigemina and Babesia bovis in cattle at 12 of the dip tanks
with the lowest tick counts at the time of bleeding were compared, the seroprevalence of
Babesia bigemina (43.6 %) was non-significantly (p=0.0912) higher than for Babesia
bovis (29.2 %). This was to be expected as the dip tanks/farms with lowest tick numbers
contained a large proportion of locations where Boophilus decoloratus was still present.
As tick numbers increased, there was a general increase in seroprevalence for both
Babesia bigemina and Babesia bovis. When the mean seroprevalences of Babesia
bigemina and Babesia bovis in cattle at 12 dip tanks with the highest tick numbers at the
time of bleeding were compared, then the seroprevalence of Babesia bigemina (55.5 %)
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was significantly (p=0.0060) lower than that of Babesia Bovis (75.9 %). The increase in
tick numbers was apparently due to an influx of Boophilus microplus.
According to Australian surveys Boophilus microplus transmits Babesia bigemina more
effectively than Babesia bovis
(Callow and Hoyte, 1961; Callow, 1964; 1967;
Mahoney, 1969; Mahoney and Mirre, 1971; Mahoney et al., 1973; Callow et al., 1976a;
Mahoney et al., 1981; Büscher, 1988; Bock et al., 1999a; 1999b). In the present survey
the transmission of Babesia bigemina appeared to decline, as Boophilus microplus
became more numerous. The findings in 5. 1. 3, 5. 5. 4 and 5. 5. 5 may be due to the
fact that Boophilus microplus transmits Babesia bigemina less effectively than it
transmits Babesia bovis (Norval et al., 1983). More research is needed on how
Boophilus microplus transmits Babesia species in Africa.
5. 5. 6. Changes in seroprevalence of Babesia bovis and Babesia bigemina in the
cattle at single dip tanks/farms where displacement of Boophilus decoloratus by
Boophilus microplus was monitored. The number of dip tank/farms where both
Boophilus species occurred was low (n=8).
•
At Modderfontein Farm both tick species were found at the first
sampling in May 1999 and Boophilus decoloratus was still present in
small numbers in December 2000. The seroprevalence on this farm
reflected the change in the tick population; in 1999, 60 % of the herd
was positive to Babesia bovis and 65 % was positive to Babesia
bigemina. By 2000, 66.7 % of the herd were positive to Babesia bovis
whilst only 30 % were now positive to Babesia bigemina.
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•
Naboomkop Farm initially had low seroprevalence to Babesia bovis
(10 %) and higher seroprevalence of Babesia bigemina (53.3 %), and
there were few Boophilus ticks present. In 2000, Boophilus microplus
had displaced Boophilus decoloratus and the seroprevalence to Babesia
bovis had increased to 48.3 % and the seroprevalence to Babesia
bigemina had increased to 65.0 %. The latter increase may have been due
to a sharp increase in the Boophilus numbers.
•
At Tshiendeulu dip tank only 4 % of the Boophilus ticks were Boophilus
decoloratus and the serology results reflect the changes in an area where
Boophilus microplus was dominant: 76.7 % of the herd was positive for
Babesia bovis and 50 % was positive for Babesia bigemina.
•
At Sendedza dip tank the serology reflected the pattern that one might
expect in an area where Boophilus microplus was increasing, with a
prevalence of Babesia bovis (43.3 %) being lower than that of Babesia
bigemina (63.3 %). In May 1999 Boophilus decoloratus was the most
common tick at this dip tank; in December 1999 the displacement of
Boophilus decoloratus by Boophilus microplus was almost complete.
•
At Luvhanga dip tank there were few Boophilus decoloratus remaining
and the seroprevalence to Babesia bovis was higher (73.3 %) than that of
Babesia bigemina (65 %).
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•
At Thononda dip tank both Boophilus species were collected on the first
sampling but the tick numbers were low and only 98 Boophilus ticks
were collected. The seroprevalence to Babesia bovis was 63.3 % and the
seroprevalence to Babesia bigemina was 31.7 %. During subsequent
sampling, when high numbers of ticks were collected, Boophilus
microplus appeared to have displaced Boophilus decoloratus.
•
At Mphephu dip tank Boophilus microplus had almost replaced
Boophilus decoloratus, but the serology still showed a pattern with
higher seroprevalence of Babesia bigemina (65.0 %) and lower
seroprevalence of Babesia bovis (53.3 %).
•
At Keerweerder dip tank few ticks were collected and only one was
Boophilus microplus. The serology indicated low transmission of TBD
and there were no reactors to Babesia bovis. At this dip tank Boophilus
microplus may have been introduced recently.
5. 5. 7. The ability of the different Boophilus ticks to transmit Babesia species. Most
of the research on Boophilus microplus and the ability of the tick to transmit the
Babesia species has been done in Australia or with Australian strains (Callow and
Hoyte, 1961; Callow, 1964; 1967; Mahoney, 1969; Mahoney and Mirre, 1971;
Mahoney et al., 1973; Callow et al., 1976a; Mahoney et al., 1981; Büscher, 1988; Bock
et al., 1999a; 1999b). When Spickett and Malan (1978) crossed Australian and South
African strains of Boophilus microplus, they reported hybrid sterility in the next
generation. This crossing may indicate that in order to adapt to the new environment,
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the South African strain of Boophilus microplus has become genetically different from
the Asian strain originally imported into the two continents at the end of the 19th
century. In addition, one can speculate that the Australian research on the transmission
of Babesia bigemina by Boophilus microplus does not necessarily apply to the disease
transmission by the African strain of Boophilus microplus. This complex problem
merits further research.
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CHAPTER 6. CONCLUSIONS AND RECOMMENDATIONS
6. 1. 1. Conclusions on the displacement of Boophilus decoloratus by Boophilus
microplus.
When Boophilus microplus first invaded the southern part of Africa in the late 1890s, it
seemed to have been contained along the coastal areas of the Eastern Cape and
KwaZulu-Natal and the spread into the hinterland was slow. Over the years there were
occasional reports of finding Boophilus microplus in new places, but the tick did not
invade all areas which were climatically favourable to it. One can speculate that
Boophilus microplus needed time to adapt to the conditions on the new continent.
Spickett and Malan (1978) crossed Australian and South African Boophilus microplus
and reported hybrid sterility between the two strains. De la Fuente et al. (2000) used
DNA techniques to show that the genetic variation between the Boophilus microplus
strains from South America and Australia was greater than between some strains of
Boophilus microplus and Boophilus annulatus.
The above findings may indicate that the strains of Boophilus microplus from isolated
gene pools had changed considerably from the original tick imported from Asia more
than a century previously. One can speculate that these changes resulted in Boophilus
microplus gradually becoming better adjusted to the local climate and vegetation. This
adjustment may then have resulted in the rapid spread and concurrent displacement of
Boophilus decoloratus seen in parts of southern Africa since 1970 (Mason and Norval,
1980; Baker et al., 1981; Norval et al., 1983; Berkvens et al., 1998).
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Boophilus species are one-host ticks and they only spread through the movement of
cattle. Over the past 30 years there has been a paradigm shift in attitudes towards tick
burdens on cattle (Mahoney and Ross, 1972; Callow, 1977; Norval, 1982; Norval et al.,
1983). Undipped cattle are regularly moved over large distances. This paradigm shift in
the philosophy of dipping may have facilitated the spread of Boophilus microplus into
new areas at a time when the tick had become truly adapted to southern Africa.
A possible development of different levels of acaricide resistance in the two Boophilus
species may explain why Boophilus microplus seems to displace Boophilus decoloratus
in the field. Acaricide resistance develops quickly in one-host ticks (Norval et al.,
1992b), but resistance patterns of the two species collected from the same farms are not
often available (Baker et al., 1981). There is at present no reason to believe that one of
the two ticks is more resistant to widely used acaricides than the other. The
displacement process seems to be due to factors other than acaricide resistance.
Until recently, researchers have suggested that the spread of Boophilus microplus into
new areas in Africa was contained or delayed by the creation of a zone of sterile hybrids
where Boophilus decoloratus and Boophilus microplus overlap. The spread of
Boophilus microplus was supposed to be slowed down and this zone would prevent
Boophilus microplus from occupying all the climatologically favourable areas on the
continent (Sutherst and Maywald, 1985; Sutherst, 1987a; Norval et al., 1992a; De Vos
and Potgieter, 1994). Such sterile hybrids do occur when Boophilus microplus and
Boophilus annulatus interbreed (Hilburn et al., 1991; Hilburn and Davey, 1992).
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Interspecific matings between Boophilus microplus and Boophilus decoloratus in the
laboratory produced sterile eggs (Spickett and Malan, 1978). When Boophilus
decoloratus and Boophilus microplus were placed on cattle in equal numbers, the two
species showed a mating preference for their own kind (assortative mating) and only 10
% of the egg mass was sterile, presumably from interspecific mating (Norval and
Sutherst, 1986). There was no evidence that any hybrid offspring had been produced
(Norval and Sutherst, 1986).
It would appear that a viable Boophilus decoloratus/Boophilus microplus hybrid similar
to the sterile hybrids described between Boophilus microplus and Boophilus annulatus
is unlikely. One may speculate that the shorter life cycle of Boophilus microplus,
combined with a possible larger number of the Boophilus microplus males available for
mating (Mason and Norval, 1980; Hilburn et al., 1991; Hilburn and Davey, 1992), may
give Boophilus microplus a reproductive advantage over Boophilus decoloratus. The
amount of assortative mating between the two species reported by Norval and Sutherst
(1986) is uncertain (Hilburn et al., 1991). There seems to be a zone of reproductive
interference where Boophilus decoloratus and Boophilus microplus overlap, but the
experimental evidence of this zone is too small to draw any conclusion on the extent to
which it contributes to contain or prevent the spread of Boophilus microplus. The
present study suggested that reproductive interference was ineffective in preventing
Boophilus microplus from spreading when the climatic conditions were favourable. The
displacement in these areas appeared to be rapid and total.
If the EI (Sutherst and Maywald, 1985) for Boophilus microplus is low, Boophilus
decoloratus may co-exist for some time with Boophilus microplus during the
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displacement process, or it may be found on its own. When the EI for Boophilus
microplus is high, Boophilus decoloratus appears to disappear quickly when Boophilus
microplus is introduced into an area. The present distribution of Boophilus microplus in
South Africa is unknown, so mapping the presence of this tick should be a high priority.
In Africa there are large geographical areas at risk to colonization by Boophilus
microplus (Sutherst et al., 1995), should the tick continue to spread from its present
sites in the southern and eastern parts of the continent. Tanzania has already reported on
the spread of Boophilus microplus (Lynen, 2001, personal communication), and it is
known that large areas in neighbouring Kenya are suitable for tick survival (Sutherst
and Maywald, 1986). The cattle in East Africa have had little exposure to Babesia
bovis, and if Boophilus microplus becomes established, the cost to the cattle industry
could be substantial. The present study illustrates that there is a strong possibility that
Boophilus microplus can easily spread into new areas of Africa.
6. 1. 2. The association between the Ecoclimatic Indices, tick numbers and Babesia
serology recorded at each dip tank/farm.
By comparing the tick collections, Babesia serology and the EI at each locality, the
following deductions were possible.
• Dip tanks/farms with an EI between 0-4 for Boophilus microplus and
an EI between 1-10 for Boophilus decoloratus. The cattle on these dip
tanks/farms carried few Boophilus ticks and the seroprevalence for both
Babesia bovis and Babesia bigemina was low. In these areas EI was
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higher for Boophilus decoloratus than for Boophilus microplus, and the
presence of Boophilus microplus was patchy whilst Boophilus
decoloratus was more common. The dip tanks/farms in this group
included Fesekraal, Matshena, Davhana, Keerweerder, Mara, and
Zwartrandjes. The cattle on these dip tanks/farms should be vaccinated
or dipped intensively when the first Boophilus ticks appear on the cattle.
•
Dip tanks/farms with an EI between 5-10 for Boophilus microplus.
Boophilus tick numbers were higher at these locations and Boophilus
microplus was common on the cattle. Seroprevalence of Babesia bovis
was generally higher than for Babesia bigemina, and at some dip
tanks/farms the herds were approaching endemic stability to Babesia
bovis. In case of a prolonged drought the seesaw effect would be felt in
these locations. The herds at these dip tanks/farms may reach endemic
stability simply by not dipping too often and by making sure that there
are always ticks on the calves and the young cattle. The farmers should
be informed about possible changes of the Boophilus species after a
prolonged dry spell.
•
Dip tanks/farms with an EI between 11-23 for Boophilus microplus.
The cattle at these dip tanks/farms carried large numbers of Boophilus
microplus ticks and would require periodic dipping to avoid tick worry.
Some of the herds at these dip tanks/farms may reach endemic stability
to TBD by simply not being dipped too often. The high EI makes it
unlikely that the cattle will ever be free of Boophilus microplus.
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Boophilus decoloratus was still present on the cattle at some of these dip
tank/farms, but it either disappeared or the numbers were greatly reduced
during the survey.
6. 1. 3. Recommendations.
Communal dip tanks with low tick numbers. Endemic stability to TBD would
probably not be attained at communal dip tanks where very low tick numbers were
recorded. There will never be enough ticks at these dip tanks to infect all the young
cattle and make the herd endemically stable. The majority of the cattle in these herds
will be susceptible to TBD. If they become infected as adults, after ticks multiply under
favourable conditions, outbreaks of disease may occur. Farmers at these dip tanks
should vaccinate their cattle or at least be prepared to dip when Boophilus ticks appear.
In our survey this group included Matshena, Fesekraal 1 and Keerweerder. Communal
farmers in the drier areas in the northern and western part of Venda must also be
prepared for the possible incursion of Boophilus microplus during wet cycles.
Communal dip tanks with large tick numbers. At these dip tanks there should be
sufficient ticks on the cattle to achieve endemic stability to Babesia bovis. The young
cattle would need 20-40 Boophilus tick bites daily to infect them with babesiosis. Care
should be taken not to dip cattle under nine months of age too frequently, as a welldesigned dipping schedule would enhance their natural immunity to Babesia. At most of
these dip tanks Boophilus microplus was common and the cattle herds at some of these
dip tanks had reached or were close to endemic stability to Babesia bovis.
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In most of the communal areas where Boophilus microplus was absent but where
Boophilus decoloratus was common, endemic stability to Babesia bigemina was the
norm. If Boophilus microplus invades these areas, the farmers will probably experience
outbreaks of Asiatic redwater and intensive dipping will be necessary to control
Boophilus microplus. This change in dipping routines may decrease the number of cattle
that were seropositive to Babesia bigemina and this would disturb the endemic stability
for this disease.
Some of the dip tanks had already reached endemic stability to Babesia bovis. This was
sometimes not the case with Babesia bigemina, however, and breakdown of dipping
could result in clinical disease from Babesia bigemina until endemic stability eventually
would be reached.
It would appear that endemic stability to bovine babesiosis could easily be lost by one
or two seasons of poor transmission of both Babesia species. Climatic changes or any
changes in the dipping schedules could lead to lower transmission of either Babesia
species, endemic instability and outbreaks of clinical disease. Some of the dip tanks
were located in areas with few Boophilus ticks, so the young cattle would not get
enough tick bites to achieve endemic stability. These herds should be vaccinated against
TBD. Most of the communal herds in this survey should attempt to reach endemic
stability to TBD, however, and this could be achieved through minimal dipping and
other integrated control strategies. Vaccination against TBD would be too costly for
most communal farmers (Norval, 1982), as the cattle would probably have to be dipped
anyway to prevent severe tick worry.
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Commercial farms. With good management it should be possible for the commercial
farmers to achieve a minimal disease situation for Babesia bovis and Babesia bigemina
in their herds. There is a strong correlation between host density and the risk of getting
infected with Babesia species (Solorio-Rivera et al., 1999) and the host density is lower
on the commercial farms than in the communally grazed areas. Regular dipping, pasture
spelling and vaccination may be economically feasible for the commercial farmers.
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