Zeitschrift for

Z Parasitenkd (1983)69 : 551 570 Parasitenkunde

Parasitology Research

9 Springer-Verlag 1983

Review Article

A Review of the Biology and Transmission Ecology

of African Bovine Species of the Genus Schistosoma
N.O. Christensen, A. Mutani, and F. Frandsen
Danish Bilharziasis Laboratory, J~egersborg Alle 1 D, DK-2920 Charlottenlund, Denmark

Abstract. The present paper reviews the information available concerning

the biology and transmission ecology of the African bovine species Schis-
tosoma boris, S. mattheei, S. rnargrebowiei and S. leiperi. Criteria for spe-
cies identification (egg morphology, intermediate host spectra, definitive
host-parasite relationships, etc.) are listed and the geographical distribu-
tion of the four species and factors determining the relative occurrence
within their overall distributional ranges are described. S. boris and
S. mattheei occur north and south of 10 ~ S, respectively, and S. margre-
bowiei occurs mainly, and S. leiperi only, in southern central Africa.
Definitive host-related factors (susceptibility, water contact pattern, etc.)
providing the background for being a primary definitive host and the
primary definitive host spectra for the four schistosome species are de-
scribed. The primary definitive host spectrum for S. margrebowiei and
S. leiperi comprise lechwe, puku and waterbuck, for S. mattheei lechwe,
puku, waterbuck plus cattle, and for S. boris cattle and possibly also
some of the listed antelope species. In addition, wild bovines and cattle
may provide a reservoir of S. mattheei and S. margrebowiei in humans,
but wild bovines and domestic stock play no major role in the transmis-
sion of other human species of schistosomes. The intermediate snail
host spectra of S. mattheei and S. leiperi only comprise members of the
Bulinus africanus species complex; S. boris is transmitted by members
of the B. truncatus, B. africanus and B.forskalii species groups, and
S. margrebowiei is transmitted by members of the B.forskalii species
group and possibly also by members of the B. tropicus and B. truncatus
species groups. Factors determining the transmission ecology of the four
schistosome species, and thereby the epidemiology of bovine schistoso-
miasis, are discussed. Influential factors comprise environmental condi-
tions mediated via the effect of these on the size of the snail host popula-
tion and on the rate of the intramollnscan development, behavioural

Offprint requests to." N.O. Christensen

552 N.O. Christensenet al.

patterns of the definitive host population and the course of the infection
in the definitive host as related to aspects of susceptibility and level
of endemicity. The epidemiological pattern (prevalence and intensity of
infection, seasonality of transmission, etc.) is described and exemplified,
and it is finally concluded that the increasing water conservation and
changing methods of husbandry may result in bovine schistosomiasis
becoming a major veterinary problem in Africa.

Introduction
Schistosomiasis has long been recognized as a common parasitic infection
in domestic stock and wild game in Africa, but there has been little recogni-
tion of its veterinary significance. Schistosomiasis in cattle and sheep may,
however, at least under conditions favouring intensive disease transmission,
cause significant losses, not only due to high mortality and morbidity from
severe infections, but also and presumably mainly due to the less easily
recognizable long-term effects of moderate and long-standing chronic infec-
tions (Dargie 1980; Lawrence 1980; Saad et al. 1980). In addition, changing
methods of husbandry and water conservation will, in the future, create
environments very favourable for the transmission of schistosomiasis (Law-
rence and Condy 1970) and the disease may therefore become a major
veterinary problem over large parts of Africa.
Suitable drugs are not available for mass treatment of schistosomiasis
in domestic stock (Hussein 1980). Even if such drugs appear it would still
be necessary to base the prevention and control of schistosomiasis on a
profound knowledge of the epidemiology of the disease. The aim of the
present paper is to review the information available concerning the biology
and transmission ecology of African bovine species of schistosomes, and
thereby the epidemiology of schistosomiasis in domestic stock and wild
game in Africa. This information is widely scattered in the literature and
has not been reviewed recently. As far as the biology is concerned, attention
is only paid to those aspects which are of importance to the epidemiology
of the disease, and the disease as such will only be dealt with to a very
limited extent. Comprehensive reviews concerning clinical, clinico-pathologi-
cal and pathophysiological aspects of bovine schistosomiasis have been pub-
lished recently by Hussein (1973), Lawrence (1978) and Dargie (1980)~

1. African Bovine Species of Schistosomes and Criteria

for their Identification
Much controversy and considerable confusion has existed regarding the
number of valid African bovine schistosome species (see Le Roux 1961;
Pitchford 1977). Schistosoma magna (Cobbold 1859), S.faradjei (Walkiers
1928), S. spindalis vat afrieana (Porter 1926), S. curassoni (Brumpt 1931),
S. hippopotami (Thurston 1963) and S. edwardiense (Thurston 1964) are pre-
sently not considered valid species, and the various reports of S. spindalis
(Montgomery 1906) and S. japonicum (Katsurada 1904) are all believed to
Biology and Transmission Ecology of Schistosoma 553

Schistosoma bovis Schistosoma mattheei

9 1 6 9 1 6 9(
Schistosoma margrebowlei Schistosoma [eiperi

Fig. 1. Egg morphology of the four African bovine species of the genus Schistosoma (scale:
100 ~tm)

refer to S. leiperi and S. margrebowiei, respectively. At present, the following

four species, all belonging to the terminal-spined schistosome species com-
plex, are accepted as valid African bovine schistosome species: Schistosoma
boris (Sonsino 1976), S. mattheei (Veglia and Le Roux 1929), S. leiperi (Le
Roux 1955) and S. margrebowiei (Le Roux 1933).
The identification of the four valid African bovine species of schisto-
somes is primarily based on reasonably constant and well-defined differences
in the egg morphology (Lengy 1962a; Dinnek and Dinnek 1965; Pitchford
1965; Taylor 1970). However, the classification based on egg morphology
alone is supported and strengthened by differences in intermediate host
spectra (Taylor 1970; Wright et al. 1972), in definitive host/parasite relation-
ships (Pitchford 1965; Taylor and Andrews 1973; Taylor et al. 1973) and
in isoenzyme patterns (Wright et al. 1972; Southgate and Knowles 1975a;
Ross et al. 1978) and also by studies on various aspects of hybridization
(Taylor 1970; Taylor and Andrews 1973; Taylor et al. 1973). Eggs of the
four valid African bovine schistosome species are depicted in Fig. 1.

2, Intra-Specific Variation and Hybridization Among African Bovine

Schistosome Species
Intra-specific variation (strain differences) may, as demonstrated for various
human species of schistosomes, have a profound effect on the epidemiologi-
554 N.O. Christensenet al.

cal pattern and the disease picture (Webbe 1971). The information available
concerning infra-specific variations among the bovine schistosome species
is, however, limited to the demonstration that S. boris can be divided into
a North African form transmitted by Bulinus truncatus and an East African
form transmitted by B. truncatus, B. africanus and B.forskalii (Southgate
and Knowles 1975a), that isolates of S. margrebowiei from Zambia and
Botswana, respectively, differ as regards the intermediate host spectrum
(see Wright et al. 1979b) and that various isolates of the form of S. boris
transmitted by B. truncatus differ with regard to the pathogenicity to ham-
ster (Southgate and Knowles 1975a). Furthermore, the suggestion by Van
Wyk (1977) that strains of S. mattheei exist that differ in their infectivity
to humans needs experimental confirmation. Although the information
available is thus very limited, it appears that too broad generalizations
concerning the epidemiological pattern and the disease picture over wider
areas are unacceptable prior to a further elucidation of various aspects
of infra-specific variations.
In recent years much attention has been paid to hybridization between
different species of schistosomes (see Wright and Southgate 1976; Wright
and Ross 1980), but the information available does not point to hybridiza-
tion between the bovine schistosome species as being of importance for
the disease picture in the bovine host. The suggestion that natural hybridiza-
tion may occur between S. boris and S. leiperi (Dinnek and Dinnek 1965)
and between S. mattheei and S. leiperi (Pitchford 1974) has not been con-
firmed in the field, and extensive field studies in East Africa in areas where
S. boris and S. mattheei co-exist have provided no evidence of natural hy-
bridization between these two species (Dinnek and Dinnek 1965). This is
supported by the demonstration by Taylor (1970) that a strong reproductive
isolation exists between S. boris and S. mattheei with a very low viability
of the F 1 miracidial generation. S. mattheei has, however, been shown to
hybridize successfully with the human species S. haematobium and it is evi-
dent that this hybridization plays an important role for the disease picture
in the human host (see Section 4). Whether a hybrid of S. haematobium
and S. manheei is infective to the bovine host remains to be demonstrated,
and the suggestion by Pitchford and Lewis (1978) that the poor response
of S. manheei to oxamniquine treatment could be due to hybridization with
S. haematobium, which is not susceptible to the drug, therefore requires
experimental confirmation.

3. Geographical Distribution of Bovine Species of Schistosomes in Africa

The information available on the distribution of bovine species of schisto-
somes in Africa has been reviewed recently by Dinnek and Dinnek (1965)
and by Pitchford (1977). Consequently, these authors should be consulted
for references and for further details than those given in the present paper.
Maps of distribution of the four bovine schistosome species in Africa are
found in Fig. 2.
Biology and Transmission Ecology of Schistosoma 555

Schistosoma boris Schistosoma mctttheei

Schistosom~a ma rgrebowiei Schist0s0ma [eiperi

Fig. 2. Maps of distribution of the four African bovine species of the genus Schistosoma

Data available concerning the distribution of S. boris outside East Africa

are rather limited, but it appears that the species is widely distributed all
over the northern (except Egypt) and western parts of Africa, and that
in Central Africa it extends southwards to central Angola, southern Zaire
and northern Zambia. S. boris occur in East Africa in a clearly defined
zone from Sudan, Ethiopia and Somalia southwards through Uganda,
Rwanda-Burundi, Kenya and Tanzania into northern Zambia. S. mattheei
occur in a zone from eastern South Africa northwards through north-eastern
Botswana, Zimbabwe, Mozambique, eastern and northern Zambia and Ma-
lawi into southern Zaire in Central Africa and to Rwanda-Burundi and
Tanzania in East Africa. S. boris and S. mattheei thus co-exist in southern
Zaire, northern Zambia, Rwanda-Burundi and Tanzania, but studies by
Dinnek and Dinnek (1965) have shown that S. boris is normally the domi-
nant species in areas where the two species co-exist.
556 N.O. Christensenet al.

S. margrebowiei is mainly known from a small area extending from

Chobe Game Reserve in north-east Botswana through Eastern Caprivi to
south-western Zambia and southern Zaire, but the species has also a few
times been recorded outside this area, namely in Chad (Graber 1969, 1978),
in Mali (Lapierre and Hien 1973) and in north-east Zaire (Walkiers 1928).
The intermediate host spectrum of S. margrebowiei is rather broad (see Sec-
tion 6) and its primary definitive hosts (see Section 4) widely distributed
(see maps in Pitchford 1976) wherefore it has been suggested that S. margre-
bowiei is much more widely distributed in Africa than hitherto thought
(Pitchford 1976). The known distribution of S. leiperi corresponds to that
of S. margrebowiei in southern Central Africa excluding southern Zaire,
but includes besides the western corner of Zimbabwe, northern Zambia
and central southern Tanzania (Pitchford 1976). In thus follows that S. lei-
peri, S. boris and S. mattheei co-exist in northern Zambia and southern
Tanzania.
The occurrence of the bovine schistosome species within their overall
distributional ranges is commonly discontinuous and it is obvious that for
example Bulinus-free highland areas are also schistosome-free. However,
the distribution of the intermediate host snails, and thereby also the schisto-
somes, is commonly discontinuous even in lowland areas (Brown et al. 1981)
and areas also exist where no schistosomes occur in spite of the presence
of the snail hosts because the prevailing temperature conditions prevent
the completion of the intramolluscan development (Pitchford and Visser
1969; Pitchford 198]; see also Section 7). Neither climatic conditions nor
the absence of the host snail can, however, explain the absence of S. boris
in Egypt, but a possible explanation could be that the cattle population
is very small (see Section 4). In contrast, the distribution of S. margrebowiei
and S. leiperi is easier to explain because the rather limited primary definitive
host spectra of these two species preclude their occurrence outside areas
where these occur (Pitchford 1976; Pitchford and Wolstenholme 1977). Fac-
tors of possible importance for limiting the distribution of each species
within areas where more species exist might comprise unknown aspects
of competition within the snail host, differences in ecological requirements
and interspecific interactions in the definitive host (see Southgate and
Knowles 1975 a; Pitchford and Wolstenholme 1977; Wright et al. 1979 b).
In areas where the conditions are favourable for schistosome transmis-
sion, prevalence rates of S. boris and S. mattheei in cattle may occur at
a level of 40-70% and commonly higher. This has been especially well
documented in Sudan (e.g. Eisa 1966; see also Majid et al. 1980), Zaire
(Schwetz 1956), Mozambique (Santos Dias 1954), Mauritania (Marill 1961),
Kenya and Tanzania (Kinoti 1964b; Dinnek and Dinnek 1965), Chad
(Graber 1969), South Africa (Pitchford 1958, 1959, 1961; Pitchford and
Visser 1965, 1969; Pitchford et al. 1973; Appleton and Bruton 1979), Zim-
babwe (Condy 1960; McKenzie 1970) and Nigeria (Schillhorn et al. 1980),
but it is reasonable to believe that comparatively high prevalence rates,
at least focally, also occur in many other areas all over Africa. The preva-
lence of S. margrebowiei and S. leiperi in domestic stock is always very
Biology and Transmission Ecology of Schistosoma 557

low (see Section 4) but their prevalence in their primary definitive hosts
is usually very high (Pitchford 1976; Pitchford and Wolstenholme 1977).

4. Definitive Host Spectra of African Bovine Species of Schistosomes

Naturally acquired infections with all four bovine species of schistosomes
have been recorded in a very large number of African mammalians (for
a complete review, see Pitchford 1977) but it is essential, from the viewpoint
of transmission, to distinguish between "primary" and "secondary" defini-
tive hosts. Primary definitive host species are, according to the definition
by Pitchford (1976), those which can maintain a specific schistosome popula-
tion indefinitely in nature if isolated from other definitive hosts harbouring
the same schistosome species, and the requirements to be met by primary
definitive host species may be summed up as follows: (1) a high susceptibility
to a particular schistosome resulting in long-lasting infections and a high
egg output per worm pair, (2) a water contact pattern ensuring a high fre-
quency of contact with cercariae-infested water, (3)a defecation pattern
ensuring a high output of schistosome eggs in snail habitats, and faecal
characteristics ensuring a prolonged egg survival in case of deposition of
faeces outside water, and (4) a non-migratory pattern of life and a popula-
tion size exceeding a certain level (Pitchford 1976; Pitchford et al. 1973,
1974). Secondary hosts do not meet one or more of these requirements
and the infections they harbour are achieved from infections maintained
in the environment by primary definitive hosts. The infections harboured
by the secondary definitive hosts are, although the prevalence rates may
be high, commonly of low intensity and occasionally of short duration,
but the secondary definitive hosts may contribute to the maintenance of
an already established schistosome population. However, secondary defini-
tive hosts may experience severe clinical schistosomiasis if they are highly
susceptible and if they share water contact points with primary definitive
hosts harbouring infections of high intensity. This is, for example, the case
with sheep when these share drinking sites with cattle harbouring S. mattheei
(e.g. Reinecke 1970; Lawrence and Condy 1970).
According to the comprehensive review by Pitchford (1977) S. boris has
been recorded as a naturally acquired infection in horse and donkey, in
cattle, sheep, goat, camel, dromedary and pig, in multimammate mouse
and swamp rat and in a number of wild bovines, including species of cobs
(Kobus sp.). Cattle, sheep and goat are all highly susceptible, but the reluc-
tance of sheep and goat to enter water presumably leaves cattle as the
only primary definitive host among domestic stock. Whether any of the
wild bovines also serve as primary definitive hosts would depend on the
untested susceptibility of these to S. boris in that at least the cob species
found infected meet all the other requirements needed (see above). S. boris
has never been shown conclusively to be a parasite of humans, the baboon
is according to Taylor (1970) not susceptible to S. boris, and from studies
by Pitchford and Visser (1962) on the possible involvement of rodents in
the transmission of S. mattheei it may indirectly be concluded that rodents,
558 N.O. Christensenet al.

although occasionally found naturally infected with S. boris (Nelson et al.

1962), play no role in the transmission.
S. mattheei is, according to Dinnek and Dinnek (1965), an indigenous
parasite of African wild bovines, and naturally acquired infections have
been recorded in baboon and vervet monkey, in various species of rodents,
in horse, zebra, cattle, sheep and goat, as well as in a large number of
wild bovine species. From the comprehensive studies conducted by Pitchford
and Visser (1975) and Pitchford et al. (1973, 1974) it appears that water
buck (Kobus ellipsiprymnus), puku (K. vardoni), lechwe (K. lethe), cattle, and
presumably also sable antelope (Hippotragus niger), wildebeest (Connechae-
tis taurinus) and buffalo (Syncerus caffer) are primary definitive hosts for
S. mat theei. The wild bovine may therefore provide a reservoir for S. mat-
theei in domestic stock if sharing of water contact points occurs. High
prevalence of S. mattheei may occur in baboons (Pitchford et al. 1973, 1974;
McConnell et al. 1974; Pitchford and Visser 1975), but Pitchford and Visser
(1975) have concluded on the basis of extensive field studies that S. mattheei
would not be able to maintain itself in a baboon population at least when
the transmission is seasonal. Pitchford and Visser (1962) also obtained evi-
dence to suggest that rodents play no role in the transmission of S. mattheei.
The low susceptibility of humans to S. mattheei is generally believed
to prevent the parasite from reaching the stage of egg production (see Blair
1966; Pitchford 1961) but S. mattheei-like eggs are nevertheless commonly
found in human excreta (e.g. Pitchford 1959, 1961; Pitchford and Visser
1975; Schutte et al. 1980). The S. mattheei-like eggs are, however, always
accompanied by eggs of either S. haematobium or S. mansoni and convincing
experimental evidence exists to support the suggestion that the S. mattheei-
like eggs represent F 1 generation eggs from a cross between male S. haemato-
bium and female S. mattheei (Pitchford 1961; Wright and Ross 1980) or
eggs produced parthenogenetically by S. mattheei females in copula with
S. mansoni males (Taylor et al. 1969; Taylor 1970, 1971). The viability of
the parthenogenetically produced S. mattheei eggs is, however, very low
and humans therefore presumably do not play any role in the transmission
of pure S. mattheei (see also Section 2).
S. margrebowiei and S. leiperi both have a very broad definitive host
range, including a large number of wild bovines among which lechwe, puku
and water buck serve as primary definitive hosts (Pitchford 1974, 1976,
1977; Pitchford and Wolstenholme 1977). Occasional reports, all from areas
with a high prevalence in wild bovines, exist of S. leiperi in sheep, goat
and cattle and of S. margrebowiei in humans, cattle and goat, but from
data available (Dinnek and Dinnek 1965; Pitchford 1976; Pitchford and
Wolstenholme 1977) it appears that humans and cattle elicit a very poor
susceptibility as reflected in low prevalences and low-grade, short-lived infec-
tions and that the reluctance of sheep and goat to enter water prevents
them from being primary definitive hosts. Infections with S. margrebowiei
and S. leiperi in domestic stock do not give rise to any major disease prob-
lems, but infections with these species in their primary definitive hosts may
give rise to clinical disease. A list of primary definitive hosts for the four
African species of bovine schistosomes is presented in Table 1.
Biology and Transmission Ecology of Sehistosoma 559

~ ~ 0

. ~
~'~
~o~

9
,_0

c)

.< ~4

c~

c~

'-a

~D
o

b
560 N.O. Christensen et al.

5. Susceptibility of Domestic Stock and Wild Bovines to Human Species

of Schistosomes
Much attention has in recent years been paid to the possible involvement
of domestic stock, but also wild bovines, in the transmission of human
schistosomiasis. From the above discussion it follows that wild bovines
provide a reservoir for S. margrebowiei and S. mattheei in humans, and
that the same is the case for cattle as far as S. mattheei is concerned. In
contrast, the only reports, of which some need confirmation, of naturally
acquired infections with S. haematobium and S. mansoni in domestic stock
and wild bovines comprise S. haematobium in Tamworth Sow (Hill and
Onabamino 1960) and in buffalo (Basson et al. 1970), a mixed infection
of S. haematobium and S. mattheei in sheep (McKenzie 1970) and S. mansoni
in sheep (McKenzie 1970) and in water buck (Pitchford et al. 1974). Infec-
tion with S. mansoni in sheep does not give rise to egg excretion (Saeed
and Nelson 1974; Adam and Magzoub 1976), but excretion of viable eggs
has been achieved in goat (Adam and Magzoub 1977) and in calves (Saeed
et al. 1969; Hussein et al. 1970) following experimental exposures to S. man-
soni, and also in sheep (Wright et al. 1972; Christensen et al. 1982), goat
(Wright et al. 1972) and calves (Wright et al. 1972) following experimental
exposures to S. intercalatum. However, low compatibility levels appear to
exist in these parasite/host combinations. In spite of relatively high numbers
of worms, S. mansoni in goat and S. intercalatum in sheep give rise to only
negligible numbers of eggs in faeces and the susceptibility of calves to
S. mansoni is very low as reflected in low to moderately low worm establish-
ment and in an only negligible egg output. The size of the egg output
is essential from the point of view of transmission, and on the basis of
the experimental exposures conducted and the very few reports available
of naturally acquired infections, it is a well-founded assumption that domes-
tic stock and wild bovines play no major role, and presumably no role
at all, in the transmission of S. intercalatum, S. haematobium and S. mansoni.

6. Intermediate Host Spectra of African Bovine Species of Schistosomes

The snail hosts for all African bovine species of schistosomes belong to
the genus Bulinus (Pulmonata, Planorbidae, Bulininae), of which some
30 nominal species exist. The Bulinus snail species are grouped into five
species groups 1 - t h e B. africanus, B. truncatus, B. tropicus, B. forskalii and
B. reticulatus species groups - and if one considers susceptibility to each
of the bovine species of schistosomes on the Bulinus species group level,
a rather clear-cut picture appears (see below). However, a complex picture
exists on the Bulinus species level in that both non-susceptible and suscepti-
ble species, of which the latter may differ as regards the level of susceptibility
to a particular schistosome species, may occur within each species group
and in that different populations of the same snail species from an even
limited geographical area may differ markedly in the level of susceptibility
1 Brown (1980) changed the grouping of the Bulinus snail species but the old system is retained
here for the sake of simplicity
Biologyand TransmissionEcologyof Schistosoma 561

(e.g. Kinoti 1971). The possible existence of strain differences within a given
schistosome species with respect to the snail host specificity may complicate
the picture even further (see Section 2). Laboratory studies using popula-
tions of schistosomes and snails from different areas may therefore not
provide information of any definitive epidemiological relevance, and the
possible limitations of laboratory experimentation using populations of schi-
stosomes and snails from the same limited geographical area should also
be kept in mind. The search for naturally infected snails is ultimately the
only sure method of incriminating a snail population as vector for a particu-
lar schistosome in a particular habitat (Teesdale and Nelson 1958).
Within a given area more than one Bulinus species (see below) may
be hosts for a particular schistosome but the relative importance of each
of the snail species depends, apart from the level of susceptibility, on a
number of other factors such as relative abundance, seasonal variations
in population sizes, habitat preferences and so on. Thus, although B. reticu-
latus from East Africa in experimental studies has been shown to be highly
susceptible to S. boris (Southgate and Knowles 1975a), its patchy distribu-
tion and pronounced seasonal occurrence would make its overall contribu-
tion to the transmission of S. boris minimal.
In North Africa S. boris is only transmitted by B. truncatus (Southgate
and Knowles 1975a and references therein; Frandsen 1979) while in East
Africa, from Sudan in the north to Tanzania in the south, S. boris exhibits
a very broad snail host range. S. boris has thus in Sudan been shown to
be transmitted by B.forskalii, B. truneatus and B. ugandae (Malek 1969;
Majid et al. 1980) and in Ethiopia by B. abyssinicus and B. truncatus (Lo
and Lemma 1975) and numerous studies (Dowdeswell 1938; McClelland
1955, 1956; Teesdale and Nelson 1958; Kinoti 1964b, 1971; Southgate and
Knowles 1975b; Southgate et al. 1980; Mutani et al., in press) have shown
that S. boris in Kenya and Tanzania is transmitted naturally by B. nasutus,
B. truncatus, B. africanus and B. forskalii, and in Uganda by B. nasutus and
B. ugandae (Schwetz 1951 ; Berrie 1964). B. globosus have never been found
naturally infected in East Africa and although in experimental studies
(Kinoti 1964a; Southgate and Knowles 1975 a; Mutani et al., in press) this
species has been shown to be of relatively low susceptibility, the possible
contribution of this species to the transmission of S. boris in this area cannot
be excluded. On the basis of epidemiological evidence, B. tropicus has been
proposed as a host for S. bovis in Kenya (Brown 1980; Brown et al. 1981)
but experimental proof to support this is still lacking. The knowledge avail-
able regarding the distribution, relative abundance and relative susceptibility
of the various snail host species provides the basis for the suggestion that
B. africanus is the most important overall host for S. boris in most parts
of East Africa, that B.forskalii presumably also contributes significantly
to the overall transmission and that the other Bulinus species found naturally
infected focally may play an important role in the transmission.
The data at hand concerning the intermediate host spectrum of S. boris
outside North and East Africa are limited to the demonstration that B. fors-
kalii and B. senegalensis serve as hosts in Senegal and Gambia (Smithers
1956; Wright etal. 1979a), but the very wide distribution of B.forskalii
562 N.O. Christensenet al.

and B. truncatus, combined with the high susceptibility of these to S. boris

in other parts of Africa, makes it reasonable to suggest that these two
species are important hosts for S. boris in Central and West Africa. Neither
direct nor indirect evidence exists concerning the possible involvement of
B. globosus in the transmission of S. boris in these areas. Moreover, a large
number of BuIinus species other than those dealt with above occurs within
the distributional range of S. boris, but the distribution of these is rather
limited and their status as hosts for S. boris in nature remains to be demon-
strated. However, if being transmitter snails their general importance is
low due to their limited geographical distribution, but they might focally
play an important role in the transmission.
Comprehensive laboratory studies by Kinoti (1964a, 1968) and Wright
et al. (1972) have shown that S. mattheei, among epidemiologically relevant
snail species, is only compatible with B. africanus and B. globosus which
are both members of the B. africanus species group. These laboratory find-
ings, combined with field observations and with the knowledge available
on snail distribution patterns in Africa, leave no doubt that S. mattheei
is transmitted naturally by B. africanus and B. globosus and presumably
not by other snail species, but the relative importance of these two host
snails still remains to be demonstrated. The suggestion by Brown (1980)
that B. tropicus should transmit S. mattheei in parts of South Africa does
not seem to be supported by the laboratory studies conducted.
Studies by Southgate et al. (1981) have shown that only members of
the B. africanus species group are susceptible to S. leiperi, and field observa-
tions have shown that at least B. africanus transmits S. leiperi in nature
(Le Roux 1955; Pitchford 1975). Epidemiological evidence provided by
Wright et al. (1979b) strongly suggests that B. globosus also serves as a
natural host for S. leiperi, but whether other members of the B. africanus
species group also act as transmitter snails in nature remains to be demon-
strated. S. margrebowiei is, according to laboratory studies conducted by
Southgate and Knowles (1977), compatible with at least some members
of all Bulinus species groups except the B. africanus species group, but only
B. forskalii and B. scalaris, both members of the B. forskalii species group,
have been found naturally infected (Wright et al. 1979b). Nevertheless,
much evidence exists to support the suggestion that at least B. tropicus,
and possibly other members of the B. tropicus species group, act as natural
hosts for S. margrebowiei. Wright et al. (1979b) have even suggested that
B. truncatus might be the transmitter snail of S. margrebowiei in Chad. A
list of intermediate host snail species for the four African species of bovine
schistosomes is presented in Table 1.

7. Transmission Ecology of African Bovine Species of Schistosomes

The transmission ecology of the bovine schistosome species, and thereby
also the epidemiology of bovine schistosomiasis, is governed by a complex
set of variable and interacting factors which will be dealt with below. It
must, however, be stressed that the information available on some essential
Biology and Transmission Ecology of Schistosoma 563

aspects of the transmission ecology is rather limited, and parts of the follow-
ing discussion will therefore be of a rather general, and to some extent,
suggestive nature.

Seasonal Variations in the Size of the Host Snail Populations

The habitats of the host snail species may be grouped into two categories,
namely permanent (perennial streams, larger dams, lakes) and temporary
(pools, smaller dams, seasonal streams, etc.) and although some host species
seem to exhibit habitat preferences, most species may occur in most types
of habitats. Rainfall and temperature variations during the year induce
pronounced, and in temporary habitats and smaller permanent waterbodies
dramatic, population fluctuations and this may provide the background
for a seasonal pattern of transmission. Peak snail densities in most types
of habitats normally occur at the end of the rainy season and at the begin-
ning of the dry season, but occasionally also later on during the dry season
(see review by Appleton 1978). Although transmission in the permanent
habitats may occur throughout the year, it appears that the most favourable
conditions for transmission in all types of habitats, at least when considering
snail numbers, commonly occur at the beginning of and during the dry
season. This seasonality with most intensive transmission at the beginning
of and during the dry season, induced by variations in snail numbers, is
furthermore enforced by the fact that other influential factors (see below)
also provide optimum conditions for transmission during the same period.
Such a seasonal pattern of transmission has been demonstrated for S. boris
in cattle in the Blue Nile Province in Sudan (Malek 1969; Majid et al.
1980) and for S. mattheei in populations of wild bovines in Eastern Transval
(Pitchford et al. 1974).

Seasonal Variations in the Rate of Intramolluscan Development

The length of the prepatent period of all four bovine schistosome species
is in the range of 4-5 weeks when at optimal temperature conditions (Pitch-
ford and Visser 1965 ; Southgate and Knowles 1975 a, 1977; Frandsen 1979;
Southgate et al. 1980, 1981) but Pitchford and Visser (1965, 1969) have
shown that the prepatent period of S. rnattheei, and thereby presumably
also of the other species, at less optimum temperature conditions may be
prolonged for up to 20 weeks, and that the intramolluscan development
is arrested completely at even lower temperatures. The effect of temperature
on intramolluscan development may therefore, if other influential factors
are kept constant, induce the following transmission patterns: (1) intensive
transmission all year around, (2) a pronounced seasonal transmission with
no transmission during the "winter" period and a more or less intensive
transmission during the " s u m m e r " period, and (3) a less pronounced sea-
sonal pattern with intensive transmission during the " s u m m e r " period, and
a less intensive transmission during the "winter" period. The latter type
of transmission is presumably the most common as it may also be induced
564 N.O. Christensenet al.

by seasonal variations in snail numbers. The seasonal transmission of

S. mattheei in Eastern Transvaal, with intensive transmission during the
"summer'" period and less intensive transmission during the ~ winter" peri-
od, is believed to be mainly due to the effect of temperature on intramollus-
can development (Pitchford and Visser 1965, 1969) and the same is at least
partly the case as far as the seasonal transmission of S. boris in the Blue
Nile Province in Sudan is concerned (Majid et al. 1980).

Daily Variations in the Number of Cercariae

in the Host Snail Habitat
Shedding of cercariae of S. leiperi occurs primarily around sunset with a
little shedding during the night. S. margrebowiei has shedding peaks around
sunrise and sunset with some shedding throughout the day and occasionally
during the night (Pitchford and Du Toit 1976). In contrast, shedding of
cercariae of S. boris and S. mattheei occurs during the early part of day
if the temperature is high and around or shortly after noon if the temperature
is low, but cercariae of S. mattheei may also, especially at low temperatures,
be shed during the night (Lengy 1962 a; Malek 1969; Pitchford and Visser
1966; Pitchford et al. 1969). Moreover, Pitchford et al. (1969) have shown
that the number of S. mattheei cercariae shed per day per snail increases
in relation to the maximum temperature of the day, that only moderate
numbers of cercariae are shed at temperatures below 20~ and that no
shedding takes place below 17~ C.
From the cercarial shedding patterns it follows that the number of cercar-
iae, and thereby the transmission potential of the habitat, may differ from
day to day depending on the daily temperature conditions, and that the
number of cercariae in the habitat is not constant throughout the day.
The time of the day at which the water contact occurs is therefore of great
importance from the viewpoint of transmission. Pitchford and Du Toit
(1976) have even suggested that the low prevalence of S. leiperi in domestic
stock, apart from their low susceptibility and the reluctance o f sheep and
goats to enter water, could be due to the fact that shedding of S. leiperi
cercariae occurs at times of the day when their water contact is minimal.
Maximum numbers of S. boris and S. mattheei cercariae in stagnant waters
occur from late morning to mid afternoor~, but in running waters the cercar-
iae are swept downstream and therefore do not accumulate at the point
of release. However, studies conducted mainly on the cercariae of human
species of schistosomes (see Jordan et al. 1980), but also on cercariae of
S. mattheei (Pitchford and Visser 1965), have shown that schistosome cercar-
iae may be carried for a considerable distance downstream without loosing
their infectivity, especially when no obstructions in the form of pools and
dense water plant beds are present. At least light infections may therefore
be achieved downstream from the point of cercarial release.

Course of the Infection in the Definitive Host

Age profiles of prevalence of S. boris in cattle in an area of high endemicity
in Sudan show a prevalence approaching 90% in animals aged 1.5 years
Biologyand TransmissionEcologyof Schistosoma 565

and a marked decline with increasing age to a level of only 30% in animals
aged 10 years or more (Majid et al. 1980). The size of the egg output is
also high in young animals and low in older animals. In areas of high
endemicity young animals are therefore primarily responsible for the trans-
mission. Furthermore, the young animals harbouring young primary infec-
tions play the greatest role because the egg output, which may reach the
level of 1,000 eggs/g faeces in young infections, becomes dramatically re-
duced 2-3 months following patency to only 10-20 eggs/g faeces (see Law-
rence 1978 ; Dargie 1980). In addition, animals harbouring chronic infections
with both S. boris and S. mattheei develop a solid resistance to reinfection,
particularly when egg output is applied as the criterion (Lawrence 1973;
Bushara et al. 1980), and the size of the egg output consequently remains
low even in the case of repeated re-exposures. However, in areas of lower
endemicity, with a less clear-cut transmission picture, older animals may
also harbour heavy infections with high egg output and an accompanying
severe disease condition, and such older animals may in these areas be
responsible for, or at least contribute significantly to, the transmission. This
has for example been the case in some of the outbreaks of clinical bovine
schistosomiasis reported as these have occurred on farms where dairy cows
were apparently responsible for the transmission (Hurter and Potgieter 1967;
Reinecke 1970; Lawrence and Condy 1970). In areas of low endemicity
may older animals thus suffer from clinical schistosomiasis, but in areas
of high endemicity clinical schistosomiasis is generally experienced only by
the young stock (see Dargie 1980).

Behavioural Patterns of the Definitive Host Population

Sheep, goats and cattle are all highly susceptible to S. boris and S. mattheei
but the reluctance of sheep and goats to enter water leaves cattle as the
only primary definitive host among the domestic stock (see Section 4). Sheep
and goats that have no contact with cattle therefore normally harbour no
schistosome infections, but if sheep and goats share water contact points
with infected cattle high and often very high prevalence rates may occur.
The reluctance of sheep and goats to enter water makes the percutaneous
route of infection of minor importance, and most infections are therefore
presumably achieved by the peroral route of infection while drinking. The
efficiency of the peroral route is, however, less than that of the percutaneous
route of infection (Lengy 1962b; Van Wyk et al. 1974; Kassuku et al., in
preparation) and only intensive transmission conditions, with high cercarial
concentrations in the water, will allow heavy infections to be established.
Outbreaks of clinical bovine schistosomiasis are therefore usually linked
to outbreaks of clinical bovine schistosomiasis, which only occur at
especially intensive transmission conditions (see Strydom 1963; Reinecke
1970; Lawrence and Condy 1970). It is presumed that cattle mainly achieve
the infection by the percutaneous route of infection, but outbreaks of clinical
schistosomiasis caused by S. mattheei have been reported in herds of cattle
which had no access to natural waters but which were watered from drinking
troughs harbouring large populations of infected host snails (Lawrence and
566 N.O. Christensen et al.

Condy 1970; Van Wyk et al. 1974). The peroral route of infection should
therefore also be considered of importance for cattle allowed to enter natural
waters freely.
The type of watering used by domestic stock plays an easily recognized
and very important role for the transmission of schistosomiasis. A clear-cut
correlation normally exists between the prevalence/intensity of infection and
the suitability of the drinking site(s) to support snail populations. This corre-
lation has for example been demonstrated by Appleton and Bruton (1979),
who within a limited geographical area found a high prevalence of S. mat-
theei in herds of cattle watered in ponds and streams, and a low prevalence
in herds watered at oligotrophic lake shorelines. Pitchford et al. (1973) also
demonstrated a high prevalence/intensity of infection with S. mattheei in
herds of cattle watered in natural waters, a lower prevalence/intensity in
herds watered from troughs and with only occasional access to natural
waters, and no infections in herds solely watered from regularly cleaned
troughs. Moreover, the higher the definitive host population, the higher
the possibility for transmission, and especially intensive transmission may
occur when the number of animals is high and the water resource limited
(Pitchford et al. 1974). This is furthermore enforced by the fact that small
waterbodies commonly provide optimal conditions for the snail host popula-
tion and the intramolluscan development (see above). It is beyond doubt
that such conditions of intensive transmission provide the background for
most of the outbreaks of clinical bovine schistosomiasis recorded (e.g. Stry-
dom 1963; Eisa 1966; Lawrence and Condy 1970; Lawrence and McKenzie
1972; Van Wyk et al. 1974; Lawrence 1977a, b). The increasing water con-
servation in the form of small dams which are suitable for snail colonization
and the accompanying increase in the cattle population thus create ample
opportunities for intensive transmission, and it is therefore reasonable to
suggest that schistosomiasis in domestic stock will become a major veteri-
nary problem over large areas of Africa.
Acknowledgements. This study was supported by a grant from the Danish International Devel-
opment Agency through a research scholarship to A. Mutani.

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Accepted May 17, 1983 "