Gillies, M.T.

English

Digital Library of the Tanzania Health Community

154 
TRANSACTIONS OF THE ROYAL SOCIETY OF 
TROPICAL MEDICINE AND HYGIENE. 
Vol. 58.  No.  2.  March, 1964. 
THE ROLE OF SECONDARY VECTORS OF MALARIA IN NORTH-EAST 
TANGANYIKA 
M. T. GILLIES* 
(From  the East  African Institute of Malaria  and  Vector  borne Diseases, Amani, Tanganyika. 
Besides the main. vectors, Anopheles gambiae Giles and A. funestus Giles, a number of 
species of anopheles are known  to play  or  suspected of  playing  a minor  part  in malaria  trans- 
mission in tropical Africa.  Where these secondary vectors  are also  exophilic in habits 
their potential role assumes greater importance, particularly following the introduction of 
the policy of malaria eradication by residual house spraying.  In accordance with their 
domestic  habits, transmission by  the main  vectors should normally be  eliminated completely 
or  reduced  to a  very  low  level.  On  the  other  hand,  it might  be  expected  that  the  other  species 
would be exposed to hazards of an altogether much lower order.  In the presence of a 
"  crash"  eradication  programme a  relatively  inefficient  but  exophilic  vector,  provided 
it was sufficiently abundant, might be able to reproduce one or two infections before the 
gametocyte  rate fell to a  low  level, and  thus preserve a  marginal reservoir of  parasites till the 
return of  the main  vectors after the campaign  has ended.  However  probable  or improbable 
such  a  sequence  of  events might  be, it is clear that one  must  have  adequate  data on  the  infec- 
tion rates and  contact with man  of  the suspected species.  This  paper, accordingly, records 
the results of salivary gland dissections made in several common species of East African 
anopheles during the 3-year period from 1959-1962.  The work was carried out in Tan- 
ganyika  at Muheza, 25 miles inland from  the coast at Tanga, details of  the topography and 
climate of which have already been given in an earlier paper in this series  (GILLIES and 
WILKES, 1963).  The  gland dissections were  carried out  in conjunction with studies on  age 
composition, both investigations being designed to provide information on the potentiality 
of these species as vectors of malaria 
The  mosquitoes were caught on human  bait outdoors at night, and  thus represented a 
very different section of the anopheline population from that found resting in houses by 
day.  A  number of catches were also made indoors, but so few specimens were caught 
other than of the main vectors that it was clear that the role of secondary vectors, if such 
existed, must be confined to outdoor situations. 
Malaria  in  the  Muheza  district  is holoendemic,  transmission  being  maintained  throughout 
the year at a very high level by A. gambiae and A. funestits, (DAVIDSON and  DRAPER, 1953; 
GILLIES,  1954), with mean sporozoite rates in the region of 5-7 per cent. for the former 
and 1-3 per  cent. for the  latter species.  The  Plasmodium  falciparum  gametocyte  rate ranged 
from 30-40 per cent. in small children to 1  per cent. in adults.  No  control measures were 
in force. 
* I am  indebted to Mr. T.  J. Wilkes  for assistance in supervising  this work, and  to Messrs. F. L. 
Ojjiki, S.  A. Magayuka  and  A.  Sabuni  who  carried  out  most  of  the  dissections  and  examinations  recorded. M. T.  GILLIES  155 
RESULTS 
The  results of  all gland  dissections carried out  are shown  in Table  I, discussion of  which 
follows. 
TABLE I.  Results of gland dissections in anopheles from Muheza  district,  Tanganyika, 1959-1962. 
Species 
A.  tenebrosus D6n. 
A. constant Lav. 
A.  pharoensis Theo. 
A. squamosus Theo. 
A.  marshalli Theo. 
A.  rivulorum Leeson 
A.  Raludis Theo. 
Numbers 
dissected 
4585 
567 
1040 
1060 
194 
147 
33 
positive 
￿ 
1 
1 
1 
￿ 
￿ 
￿ 
Anopheles  coustani  group. 
By  far  the  largest number  of  dissections  was  of  Anopheles  tenebrosus, yet  no  positive  glands 
were  found.  On  the other hand  one  infected gland was  found among  some  500 A. coustani 
examined.  This  finding suggests a  difference in vector  potentiality between  the  two  species, 
a view  that finds support from  the results of dissections in other parts of Africa shown  in 
Table II.  It will be  seen that up  till now  all the infected specimens from  this group have 
TABLE II.  Summary  of records of gland dissections in Anopheles coustani group. 
Species 
A. tenebrosus 
A. coustani 
-
 
A. ssiemanni 
A.  siemanni  1 
A.  coustani  j 
Country 
Natal 
Mozambique 
Katanga 
Tanganyika 
Katanga 
Tanganyika 
Katanga 
Ethiopia 
Cameroons 
Upper  Volta 
Author 
De  Meillon (1947) 
Vincke (1947) 
Present  series 
Vincke (1947) 
Present  series 
Vincke (1947) 
Giaquinta Mira  (1950) 
Adam  (1956) 
Hamon  and Mouchet  (1961) 
Number 
dissected 
377 
172 
4585 
1135 
567 
1035 
? 
119 
3385 
Number 
positive 
- 
￿
 
￿ 
i 
i 
- 
i 
i 
3 556  ROLE OF SECONDARY VECTORS OF MALARIA IN TANGANYIKA 
belonged to A. constant or Anopheles siemanni.  This difference in infectivity is paralleled 
by differences in nulliparous rates, the observations of HAMON  (1963) and GILLIES (1963) 
indicating that populations of A. tenebrosus are significantly younger. 
These  findings  call for some  comment  on  the  systematic  status  of  the  various  members  of 
the A. coustani group, which have been regarded by most authors as simple’"  varieties,". 
i.e., variants within a single polymorphic  species.  This view point has been supported by 
workers in certain parts of West  Africa where specimens intermediate between A. coustani 
(s.str.) and A. sdemami commonly occur (HAMON, et al.  1956).  However, in East Africa 
the  three forms mentioned here show  striking differences in relative abundance  in time and 
place, and  intermediates rarely occur, even  in  areas  where  all three  are  sympatric.  This  fact, 
taken  in conjunction with  the difference in survival and  infection rates observed in A. tene- 
brosus, indicates the importance of recognizing the specific distinctness of at  .least the latter 
form. 
Filarial larvae were occasionally observed in both members of the A. coustani group. 
Infection rates were  usually low, although in one  series of 860 A. tenebrosus there were  five 
.
  positives.  One  of  these  larvae  was  examined  by  Dr. G.  S. Nelson  of  the  Insect-Borne  Diseases 
Division, Kenya, who  reported  that  it belonged  to the genus  Dirofilaria and  was  thus  clearly 
of  animal origin.  Filarial infections in A.  tenebrosus were  recorded  by  MUIRHEAD-THOMSON 
(1951) from  Dar-es-Salaam.  In  this case, also  the  definitive host  of  the worm  was  unknown. 
Another member of the A. coustani group. Anopheles paludis Theo., which has been 
reported as a  vector  in the Congo  with sporozoite rates as high  as 10  per  cent., (Lips, 1961), 
was  a  scarce mosquito  at Muheza  and  no  positives were  found  in the small series dissected. 
But  it may  be  noted  that the  proportion nulliparous  in these specimens was  of  the  same  high 
order  as in others of  the group.  ,, 
Anopheles  pharoenyis. 
A  single positive was found in about 1000 dissections at Muheza.  Elsewhere in East 
Africa GIBBINS (1932) recorded one positive out of 150 in Uganda, GAENHAM  (1945) none 
out  of  1334  dissections at Kisumu  in Kenya, DRAPER  and SMITH  (1957) one  out  of  about  500 
in the Pare district of Tanganyika, and CLYDE and WEBBE  (1955) none out of about 500 
from Mpanda in south-west Tanganyika.  In West Africa infected glands are not un- 
commonly  found, though always at very low rates 
￿
 (HAMON and MOUCHET,  1961) ;  while 
in Egypt  it is well known  as an  important  vector, although again usually with very low  in- 
fection rates.  HAMON  and  MOUCHET  (loc. cit.) made  the suggestion that this low  infectivity 
was  at least partly due  to low  survival rates in nature, a  view  that is strongly supported by 
the high nulliparous rates of 55 and 54  per cent. reported from West  and  East Africa, res- 
pectively, (HAMON, 1963;  GILLIES,  1963).  Recent observations on the age composition 
of A. pharoensis in Egypt by  ZAHAR  et al. (1962), using Polovodova’s technique for age de- 
termination, (DETINOVA,  1962),  have amply illustrated the short-lived nature of Egyptian 
populations of  the  species.  Thus  it seems  highly  probable  that  the  same  attribute character- 
izes equatorial populations of  this mosquito. 
Both GARNHAM  (1945) and DRAPER and SMITH (1957) have raised the question as to 
whether the sporozoites observed were in reality of human  origin.  While it  is obviously 
impossible to be sure in any individual case, the known  vectorial role of A. pharoensis; in 
Egypt  (BARBER and RICE, 1937), often in the absence of any other proved  vector, the wide- 
spread occurrence of  infections in other parts of  Africa and  its known  high susceptibility to M. T.  GILLIES^  157 
infection in the laboratory (HAMOM and MOUCHET, 1961), all point to the conclusion that 
most  of  the  infections observed must  be  regarded as of  human  origin until contrary evidence 
is  produced. 
Anopheles squamosus (sensu stricto). 
One  positive gland was found in about 1000 dissections at Muheza.  This appears to 
be the first gland infection observed in A. squamosus, although few dissections have been 
recorded by other workers (DE MEILLON, 1947).  VINCKE  (1946) dissected 256 females in 
Katanga  without  finding any  positives, although he  found  one  oocyst  in a  specimen  dissected 
5 days  after capture. 
Observations on the age composition of A. squamosus have yielded similar results to 
those on A. pharoensis, the rates of 60 per cent. and 65 per cent. nulliparous recorded from 
West and East Africa (HAMON, 1963;  GILLIES,  1963), being if anything even higher than 
in  the  latter species. 
DISCUSSION 
These observations show clearly the negligible importance of secondary vectors in the 
East African area concerned.  With  the exception of A. tenebrosus, which was never found 
.
 
infected, the numbers  of  the other species caught  biting man  was  nearly always  low.  Thus, 
even when  the chance  of  contact with man  of exophilic mosquitoes was  artificially raised by 
placing the catchers outside after the inhabitants had retired indoors, the amount of  trans- 
mission  taking place was  always  of an  exceedingly low  order.  Although  quantitative catches 
were  not made, the material collected by  two men  working on"  piece rates " for 1-2 hours 
a night, five nights a week  for a minumum  of 48 weeks a year, provided a not unrealistic 
picture of the exposure to attack by  exophilic mosquitoes experienced by  the population at 
large.  Yet  their activities yielded only one infected  specimen per annum.  By contrast, 
A.  gambiae  and  A.fumstus  in  the  same  village  were  estimated  to  have  subjected  each  inhabitant 
to 220  infective bites a  year (GILLIES, 1954).  This  makes  it clear that, once  house  spraying 
is in force, it would be virtually impossible for secondary vectors to maintain transmission 
except as the rarest of accidents.  Such accidents are likely to be of minor significance 
compared with the many other difficulties that beset eradication programmes.  The same 
conclusion was reached by HAMON  and MOUCHET  (1961) in their review of the position in 
West Africa and elsewhere, and it seems fairly safe to assume that, outside strictly local 
situations, there is little fear that the presence of non-domestic,  secondary vectors will be a 
serious impediment to eradication schemes in Africa. 
A  common  feature of  the biology of  the species considered here  is their relatively short 
span of  life, with natural mortalities estimated by GILLIES (1963) to be  of  the order of  50  to 
70  per  cent. per  gonotrophic  cycle.  Although  we  have  little  precise  information  on  the  degree 
of contact between man  in his natural setting (as opposed  to baits deliberately placed out  of 
doors) and most exophilic mosquitoes, it is apparent that mortalities of this order must  in 
themselves severely limit their capacity to act as vectors of disease. 
SUMMARY 
Single sporozoite positive specimens of A.  coustani,  A. pharoensis and A. squamosus 
were found among series of dissections made in the course of a 3-year study of infection 
rates in outdoor  biting anopheles.  No  infected specimens  were  found among  large numbers 158  .ROLE OF SECONDARY  -VECTORS OF MALARIA IN TANGANYIKA 
of A. tenebrosus dissected.  Apart from the latter species,  all the others were present in 
relatively small  numbers.  It  is concluded  that  none  of  them  is likely  to be  of  any  importance 
once  transmission by  the main  vectors has been  interrupted.  Their poor  vectorial capacity 
appears  to be  linked with a  naturally occurring high mortality rate. 
REFERENCES 
ADAM,  J.-P. (19S6).  Bull. soc. Path. exot., 49, 210. 
BARBER, M.  A. &  RICE, J. B. (1937).  Amer.  J. trap. Med., 17, 413. 
CLYDE, D. F. &  "WEBBE, G.  (1955).  In Annual  Report, Medical  Department, Dar  es Salaam. 
DAVIDSON, G. &  DRAPER, C. C. (1953).  Tram.  R. Sac. trap. Mod.  Hyg., 47, 522. 
DETINOVA,  T.  S. (1962).  Age-grouping  methods  in  Diptera  of medical  importance. 
’ 
Geneva  :  W.H.O. 
DRAPER, C. C. &  SMITH,  A. (1957).  Trans. St. Soc. trap. Mod.  Hyg., 51, 137. 
GARNHAM,  P. C. C. (1945).  Ann. trap. Med.  Parasit., 39, 63. 
GIAQUINTA  MIRA, M.  (1950).’  Riv. Malarial., 29, 281. 
GIBBINS, E. G.(1932).  Am.  trap. Med. Parasit., 26, 239. 
GILLIES, M.  T.  (1954).  Ibid., 48, 58. 
.￿￿￿￿,(1963).  Jh’A,57,435. 
￿￿￿￿  &  WILKES,  T.  J., (1963).  Ibid., 57, 204. 
HAMQN,  J. (1963).  Bull. World  Hith. Org., 28,83.-  ￿￿￿￿,  ADAM,  J.-P. &  GRJEBINE, A. (1956).  Ibid., 15, 549. 
￿
￿
￿
  &  MOUCHET,  J. (1961).  Med.  trap., 21, 643. 
LIPS, M.  (1961).  Riv. Parassit.. 23, 275. 
DE  MEILLON,  B. (1947).  Publ. S. Afr.Inst. Med.  Res., No.  49. 
THOMSON,  R. C. MUIKHEAD,  (1951).  Bull. ent. Res., 41, 487. 
VINCKE, I. H.  (1947).  Ann. Soc. beige Med.  trap., 26, 385. 
ZAHAR, A. R-, ZAGHLOUL, Ezz EL-ARAB &  THYMAKIS, K. (1962).  Unpublished Report, Regional 
Malaria  Eradication Training  Centre, Cairo.  ’ 

The Role of Secondary Vectors of Malaria in North-East Tanganyika

http://ihi.eprints.org/1294/1/ifakara(45).pdf

The Role of Secondary Vectors of Malaria in North-East Tanganyika

Abstract

Similar works

Full text

Available Versions

Digital Library of the Tanzania Health Community