The Physiology of Mosquitoes

411 Pages·1963·9.5 MB·English

by  A. N. Clements and G. A. Kerkut (Auth.)

OTHER TITLES IN THE ZOLOGY DIVISION
General Editor: G. A. KER K U T
Vol. 1. RAVEN — An Outline of Developmental Physiology
Vol. 2. RAVEN — Morphogenesis: The Analysis of Molluscan Development
Vol. 3. SAVORY — Instinctive Living
Vol. 4. KER K U T — Implications of Evolution
Vol. 5. TARTAR — The Biology of Stentor
Vol. 6. J E N KIN — Animal Hormones — A Comparative Survey
Vol. 7. CORLISS — The Ciliated Proto^pn
Vol. 8. GEORGE — The Brain as a Computer
Vol. 9. A R T H U R — Ticks and Disease
Vol. 10. RAVEN — Oogenesis
Vol. 11. M A N N — Leeches (Hirudinea)
Vol. 12. SLEIGH — The Biology of Cilia and Flagella
Vol. 13. PITELKA — Electron-Microscopic Structure of Protozoa
Vol. 14. FINGERMAN — The Control of Chromatophores
Vol. 15. LAVERACK — The Physiology of Earthworms
Vol. 16. H A D Z I — The Evolution of the Meta^pa
OTHER DIVISIONS IN THE SERIES ON
PURE AND APLIED BIOLOGY
B I O C H E M I S T R Y
B O T A N Y
M O D E R N T R E N D S
I N P H Y S I O L O G I C A L S C I E N C E S
P L A N T P H Y S I O L O G Y
THE PHYSIOLOGY OF
MOSQUITOES
BY
A. N. CLEMENTS
Department of Physiology and Biochemistry
University of Southampton
PERGAMON PRESS
OXFORD · LONDON · NEW YORK · PARIS
1963
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THE BAY TREE PRESS, STEVENAGE, HERTS
A C K N O W L E D G E M E N T S
O N E of the pleasures of writing this book has been the contact with the
many people who have helped me during its preparation. To name only
a few, J. D. Gillett, J. C. Jones and J. J. Laarman have made a most
valuable contribution by reading and criticizing parts of the manuscript,
and A. W. A. Brown, A. J. Haddow, A. O. Lea, P. F. Mattingly and
E. T. Nielsen have helped me in a variety of ways. To these and the
many others I express my gratitude. I am also greatly indebted to Miss
Barbara Trott, Librarian of the Commonwealth Institute of Entomology,
for much assistance. Thanks are due to D. S. Bertram and R. G. Bird
and to the Editors of the Transactions of the Royal Society of Tropical
Medicine and Hygiene for permission to reproduce electron micrographs,
which form a valuable addition to the book.
I am grateful to the following publishers for permission to reproduce
illustrations: Akademie-Verlag G.m.b.H. {Deutsche Entomologische Zeit-
schrift) \ Akademische Verlagsgesellschaft Geest und Portig K.-G.
{Zoologisches Anzeiger)', American Entomological Society {Entomological
News) ; American Institute of Biological Sciences {Entomological Review) ;
British Museum (Natural History) (Edwards, Mosquitoes of the Ethiopian
Region; Lang, A Handbook of British Mosquitoes; Marshall, The British
Mosquitoes) ; Cambridge University Press {Journal of Experimental Biology;
Parasitology; Christophers, Aedes aegypti); Clarendon Press, Oxford
{Quarterly Journal of Microscopical Science); Commonwealth Institute of
Entomology {Bulletin of Entomological Research); Ecological Society of
America and Duke University Press {Ecology); Ejnar Munksgaard Ltd
{Oikos) ; Elsevier Publishing Company (Tropical and Geographical Medicine) ;
Entomological Society of America {Annals of the Entomological Society of
America); VEB Gustav Fischer Verlag {Zoologische Jahrbucher); S. Hirzel-
Verlag {Acustica); Imprimerie Albert Kundig (Revue Suisse de Zoologie);
Indian Journal of Medical Research; Macmillan & Co., Ltd. {Nature); Ohio
State University and Ohio Academy of Science {Ohio Journal of Science) ;
Presses Universitaires de France {Bulletin Biologique de la France et de la
Belgique) ; Royal Entomological Society of London {Proceedings and Transac-
tions of the Royal Entomological Society of London); W. B. Saunders Co., Ltd.
(Boyd, Malariology) ; Smithsonian Institution {Smithsonian Miscellaneous
Collection); Springer-Verlag {(österreichische Zoologische Zeitschrift, Wilhelm
Roux' Archiv für Entwicklungsmechanik der Organismen, Zeitschrift für
vin
ACKNOWLEDGEMENTS IX
Morphologie und Ökologie der Tierey Zeitschrift für Vergleichende Physiologie) ;
Stanford University (Microentomology) ; Tohoku University (Science Reports
of Tohoku University); University Press of Liverpool {Annals of Tropical
Medicine and Parasitology); University Press, Notre Dame, Indiana
(American Midland Naturalist) ; Verlag Birkhäuser AG (von Buddenbrock,
Vergleichende Physiologie); Verlag für Recht und Gesellschaft A.G. (Acta
Tropica); Verlag der Zeitschrift für Naturforschung (Zeitschrift für
Naturforschung); Wistar Institute of Anatomy and Biology (Journal of
Morphology); World Health Organization (Bulletin and Monograph of the
World Health Organisation).
CHAPTER 1
THE EGG
Embryonic Development
Mosquito eggs are elongate and bilaterally symmetrical and bounded by
a thick shell which is pierced at the anterior pole by the micropyle. The
newly-laid egg is filled with yolk granules separated from one another
by a fine cytoplasmic network while a thin layer of cytoplasm free of yolk
granules, the periplasm, is found under the shell, being thicker at the
anterior and posterior poles. The bigger yolk granules are composed of
protein (Nicholson, 1921) and between these are many small fat droplets
associated with Golgi apparatus (Nath, 1929). At the posterior pole is a
saucer-shaped heavily-staining region of pole plasm. Before fertilization
the nucleus lies in a small volume of yolk-free cytoplasm, situated towards
the anterior pole in Anopheles maculipennis (Ivanova-Kazas, 1949) and
about the middle of the egg and near the surface in Cuiex pipiens (Idris,
1960a).
Sperm are thought to pass through the micropyle as the egg traverses
the genital chamber at oviposition. Polyspermy is normal in Culex
pipiens, many sperm penetrating the egg but only one fertilizing it. The
eggs of Culex pipiens are usually laid during the first maturation division
of the oocyte nucleus, sometimes during the second. After the second
maturation division the female pronucleus migrates to the centre of the
egg, and the polar bodies, consisting of the other daughter nuclei of the
meiosis, remain in the periplasm and later degenerate. At 21 °C fusion
of male and female pronuclei occurs 30-45 min after oviposition
(Idris, 1960a).
Five divisions convert the zygote nucleus to a group of 32 cleavage
energids in the centre of the egg, each consisting of a nucleus embedded
in a small volume of cytoplasm (Fig. 1). The following 2 divisions yield
a sphere of 64 and then 128 energids which migrate with their cytoplasm
towards the surface. At the 128-nuclei stage in Culex pipiens & small
number of cleavage energids penetrate the pole plasm, absorbing some of
its basophilic material, and continue their migration to the posterior pole.
After the next division the ooplasm withdraws from the posterior pole
leaving a liquid-filled space into which pass those cleavage energids which
1
2 THE PHYSIOLOGY OF MOSQUITOES
(a) (c)
sperm
-sperm
cleavage
' energids
oocyte
nucleus
pole plasm
(d)
blastoderm
forming
cephalic
<7
fv '·' groove
vitellophags
pole cells
F I G . la-f. Cleavage and blastoderm formation in Culex pipiens.
(a) Egg before cleavage; (b-d) certain stages from 1st to 8th cleavages; (e)
preblastoderm stage (cf. Fig. 2a); (f) blastoderm at start of differentiation
(cf. Fig. 2c). (From Idris, 1960a).
THE EGG 3
have penetrated the pole plasm, now visibly differentiated as spherical
pole cells. These by division form a group of approximately 12 pole cells
(Fig. Id) (Idris, 1960a). In Anopheles maculipennis 4 cleavage energids
normally penetrate the pole plasm and by division form a group of 20-30
pole cells (Ivanova-Kazas, 1949). The 8th division, which occurs shortly
after the mass of cleavage energids have penetrated the periplasm, should
theoretically yield 256 nuclei but in Culex pipiens approximately 16 nuclei
remain dispersed in the yolk becoming vitellophags and these do not
divide simultaneously with the others. The periplasm doubles in thickness
during the early cleavages.
Owing to the position of the fusion nucleus cleavage starts near the
anterior pole in Anopheles maculipennis (Ivanova-Kazas, 1949) and near
the middle of the egg in Culex pipiens (Idris, 1960a). In Culex pipiens eggs
at 18°C the number of nuclei increases logarithmically during the first
3 hr with a division every 20 min but after that time, when blastoderm
formation starts, the rate of cleavage falls off (Christophers, 1960).
Development proceeds at a similar rate in Anopheles maculipennis (Ivanova-
Kazas, 1949). Blastoderm formation starts after the 9th division when
furrows in the egg surface begin to separate the nuclei, starting near the
middle of the egg where the energids first reach the edge of the yolk. A
further division occurs and the furrows penetrate deeper into the peri-
plasm soon forming complete cell walls so that a blastoderm of columnar
cells surrounds the yolk and cuts off the group of pole cells (Fig. 2). At
this time the egg of Culex pipiens contains 35-50 vitellophags and rather
fewer than 1000 blastoderm cells (Idris, 1960a).
The blastoderm next thickens ventrally forming the germ band (Fig. 2c),
a condition which is reached in Culex pipiens after 5 hr development at
21°C (Idris, 1960a). Considerable changes take place between 5 and 20 hr
development in the dimensions and form of the germ band. It grows to
the anterior pole and also grows backwards past the posterior pole to
extend upwards and along the dorsal surface so that it almost encircles
the egg (Fig. 3a-e). Idris (1960b) considers that this extension results
from growth of the whole germ band and not simply of the caudal region,
and this is confirmed by the fact that momentary irradiation of the
posterior end of the egg during extension damages different segments
between the front and tip of the abdomen depending on the time of
irradiation (Oelhafen, 1961). Elsewhere the blastoderm becomes reduced
to a delicate nucleated membrane but as the germ band is wide this thin
region consists only of 2 narrow lateral bands linked by an area on the
dorsal surface where the caudal end of the germ band fails to reach the
head (Fig. 5) (Christophers, 1960). The embryo as a whole does not sink
into the yolk at any stage. After 10 hr development the germ band
4 THE PHYSIOLOGY OF MOSQUITOES
F I G . 2a-d. Blastoderm formation and gastrulation in Culex pipiens.
(a) T.S. through middle of embryo in preblastoderm stage; (b) T.S. through
middle of embryo in uniform-blastoderm stage; (c) T.S. towards posterior end
of embryo at start of differentiation; (d) T.S. through middle of embryo
during elongation of germ band (cf. Fig. 3c). (From Idris, 1960a).
5
THE EGG
ate
median plate
(d)
Λ*
ventral groove