June, 2003 Journal of Vector Ecology 1

Distinguished Achievement Award Presentation at the 2002 Society of Vector Ecology Meeting

Physiological bases of mosquito ecology

Hans Briegel

Institute of Zoology, University of Zürich

Winterthurerstr. 190, CH-8057 Zürich, Switzerland

Received 15 December 2002; Accepted 27 December 2002

ABSTRACT: The research carried out during more than 30 years in the author’s laboratory is briefly reviewed.
Quantitative analyses of basic physiological processes, such as growth and development, digestion and excretion,
oogenesis and fecundity, reserve synthesis and resulting flight-potentials of Aedes aegypti were summarized and
compared with several other mosquito species, particularly with Anopheles. These studies led to the recognition
of distinctly different physiological strategies, for which the term “physiotype” has been coined, providing a basis
for understanding the different ecotypes. Journal of Vector Ecology 28(1): 1-11. 2003.

Keyword Index: Reproduction, metabolism, flight, eco-physiology, strategies.

First and foremost, let me express my sincere stoichiometric relationships and principles governing
gratitude to the Society for Vector Ecology for this the metabolic events during the reproductive cycles of
prestigious Distinguished Achievement Award and for Ae. aegypti (Briegel 1985, 1990a) and Anopheles species
the opportunity to attend this meeting. It is good to see (Briegel and Rezzonico 1985, Briegel and Hörler 1993,
so many scholars of mosquito biology together again. I Klowden and Briegel 1994). Once we had quantified
also appreciate the opportunity to present a short blood ingestion, protein digestion, and excretion of the
overview of our work that has been carried out during catabolites, we had a metabolic background for entering
the last three decades, mainly in Switzerland. I will try to the field of reproductive physiology and oogenesis
draw a general and very personal picture of some (Briegel 1985, 1986, Lea et al. 1978, Briegel et al. 2002).
physiological aspects of mosquito life styles that may We then expanded to larval development (Timmermann
provide a background for a better understanding of and Briegel 1996, 1998, 1999) and to other mosquito
ecological situations encountered in the field. For that species, and we finally became entangled in the flight
purpose, I would like to point out the advantages of fully potential and energetics of female mosquitoes (Briegel
quantitative analytical procedures available in the et al. 2001a,b, Briegel and Timmermann 2001). Using flight
laboratory and what we can learn from such studies. We mills, we were able to record the flight distances, the
worked in several fields of comparative physiology with patterns of flight activity, and the utilization of reserves
different mosquito species. in comparison to pre-flight conditions and to those that
My research began with studies of blood digestion had not flown. During all phases of our research, I had
in Aedes aegypti (Briegel and Lea 1975, 1979, Briegel always intended to address and answer basic questions
1981, 1983). We clarified the enzymatic and endocrine about the mosquito and its actual behavior in the field
regulations of the processing of the blood meals (Graf and/or ecological adaptations of certain species. I will
and Briegel 1982, Hörler and Briegel 1995, 1997), and for select a few examples and results to put parts of the
the first time, achieved the purification of mosquito physiological mosaic together to reveal a picture of the
trypsin and characterized its synthetic pathway (Graf and ecophysiology of a species. In doing so, distinct
Briegel 1985, 1989, Graf et al. 1986, 1998). Because there species-specific strategies could be identified.
is no digestion without excretion, we also quantitatively The larval period of mosquitoes is a primary target
studied the excretory processes in great detail (Briegel of all control methods. Therefore, we studied their growth
1975, 1980a, b, 1986, Briegel et al. 1979, von Dungern and and development, their proteolytic enzymes, and their
Briegel 2001a,b). This led us to an understanding of synthesis of reserves (Timmermann and Briegel 1996,
 2 Journal of Vector Ecology June, 2003

Figure 1. Effect of depth of water in the larval rearing containers in five mosquito species. These containers were
rat cages (22x40 cm, 15 cm high) filled with water to depths of 0.5, 1, 2, 5, and 14 cm, each with 200 larvae. Total
eclosion of imagoes is expressed as a percent of newly hatched larvae. Optimal development was always at water
depths of 0.5 to 1 cm.

1998, 1999, Hörler and Briegel 1995, 1997). Different During the fourth and last instar, 80-90% of the growth
feeding mechanisms are commonly recognized among and biosynthesis takes place; if not enough is
various groups (Dahl 1993). We quantitatively accumulated, the larvae can wait for 2-3 weeks until they
demonstrated that mosquito larvae could utilize only a finally pupate or die. If they pupate they give rise to
narrow water segment between the water surface and small or large imagoes, while the dead larvae provide
the deeper zones (Figure 1, Timmermann and Briegel, additional food for their sisters and brothers. I say sisters
unpublished data). This observation provided a general and brothers, because during the fourth instar the sexual
understanding of mosquitoes that usually breed in differences in growth and biosynthesis become
shallow water ponds, always close to the surface or to expressed (Timmermann and Briegel 1999). Because most
the margins. Therefore, our interests were centered mosquito larvae live in stiff opposition between feeding
around the nutritional aspects. It turned out that mosquito in the water column or on the bottom and breathing at
larvae definitely require food of animal origin in addition the surface, the biosphere accessible to them is often
to plant debris (Timmermann and Briegel 1996) in order confined to only a few centimeters, particularly in the
to meet their needs for the essential poly-unsaturated Anophelines, which lack a siphon and spend most of
fatty acids that apparently do not occur in plant material, their lives at the surface (Timmermann and Briegel 1993).
as already had been shown by Dadd (1981, 1983). These constraints are reflected in variable imaginal body
Mosquito larvae feed continuously, similar to caterpillars. sizes and their teneral reserves that in turn, strongly
Some elegant endocrine mechanisms regulating molting affect the life of the imagoes (Briegel 1990b, Figure 2).
and metamorphosis in Lepidoptera have been revealed After eclosion, insects enter a shorter or longer
(Nijhout 1975), but to our surprise, mosquito larvae were “maturation period,” the teneral phase. In mosquitoes
different. While caterpillars are able to adapt their molts this lasts about one day. This is a very important period,
to their nutritional status, even through supernumerary because so many covert effects take place at all levels:
instars, this is impossible in mosquitoes. They are anatomical differentiation, behavioral maturation, the
programmed for four larval instars, and the environmental, hormonal system, the digestive system, vitellogenesis,
mainly dietary conditions, determine their final body size. and also the flight muscles. All require their time before
We found an absolute value for each instar in the diameter the true nature of the mosquito and its blood-sucking
of their head capsule (confirming Dyar’s rule with a factor habits become manifested. Among all these aspects, the
of 1.1), whereas the thorax diameter indicates the biomass quantity of teneral reserves “inherited” from the larva
acquired by the larva (Timmermann and Briegel 1998). are crucial (Figure 2, Briegel 1990a, b).
June, 2003 Journal of Vector Ecology 3

When studying the physiology of any insect, there recognized so far; autogenous females and males are
is one very important parameter to consider that is not considered at this point.
obvious but often neglected: body size. We had initiated First, let’s consider the classic case of Ae. aegypti,
rigid evaluations of mosquito body sizes in all our which has been thoroughly studied in so many respects.
research. In insects, particularly in mosquitoes, weight The linear regression for protein against body size and
determinations are often misleading except for the dry the exponential regression for lipid have been shown in
weights. Therefore, morphometric measures are always Figure 2 with the isometric and positive allometric
best, but for physiological considerations, volume and functions, respectively (Briegel 1990a). Within a few
not linear dimensions are required (Schmidt-Nielsen hours of eclosion, these females begin to take sugar if
1984). Consequently, we decided for the simplest available, thus improving their teneral lipids. When
treatment, which is the cubic value of the wing length, or deprived of sugar, they avidly take blood meals within
some other length of the exoskeleton. In this way, body one day and can survive, but not necessarily reproduce,
size is a dependable measure for these reserve conditions unless they are of large body size. Blood meals add a
that follow significant isometric or allometric substantial amount of protein. In our experiments we
relationships, although with species-specific slopes and always gave measured blood meals by enema to each
extent (Briegel 1990a, b; and Figure 2). We routinely female (0.5–5 µl), followed by individual micro-analyses
produced mosquitoes covering the whole spectrum of of intestinal enzyme activities, of the yolk components,
possible sizes in several species (Briegel 1990a, b). This and of the principal catabolites (Briegel 1985, 1986,
is easily accomplished by manipulating the food supplies 1990a). Figure 4 combines such measurements during a
and/or the population densities during the larval period. gonotrophic cycle of large Ae. aegypti. Figure 5
Different reproductive strategies are recognized. Females demonstrates the perfect synchronization amongst the
may or may not profit from the larval reserve various processes: yolk volume parallels the appearance
accumulations, and accordingly they seek additional of yolk protein and yolk lipid, whereas glycogen appears
sources. Of course, blood from vertebrates is a valuable, at the end, shortly before chorionation. Uric acid
although a difficult and dangerous source for the synthesis parallels urea formation, and both coincide
additional protein required. This is the central issue of with yolk deposition, as shown in Figure 4. All the events
hematophagy and of most investigations on mosquito taking place in such a narrow sigmoid area (hatched
physiology, besides the problems of pathogen area in Figure 4) point out the remarkable capability of
transmission. However, there is an equally important and the fat body cells to distribute the nitrogen units to
more variable story involving the synthesis and reserves synthetic mechanisms (vitellogenin) and to the catabolic
of lipids, their needs for yolk production, and their mechanisms (uricotely, ureotely, and ammonotely). In
energetic significance. addition, the carbohydrate units obtained through
Total protein always follows a highly significant and protein degradation are also converted to appropriate
linear correlation with body size because protein at this amounts of lipid synthesis. Hematin defecation marks
stage represents mainly a structural component. Lipids the end of the digestion period and was shown to be
on the other hand can follow linear correlations with regulated on a neuronal basis (Briegel and Lea,
body size, equal to protein or much higher, or they show unpublished data, Van Handel and Klowden 1996). These
exponential correlations of steep or flat inclinations measurements also allowed the determination of the
(Briegel 1990a, b). To compensate for low teneral lipids, extent of the utilization of blood for oogenesis in large
females may seek sugar sources, which then enter the and small females, and the establishment of complete
lipogenetic pathways, in most cases before blood meals protein budgets (Figure 6). As a rule, blood meal protein
are added (Briegel et al. 2001a, b). Hormonal factors is always ingested in surplus of the need for
suppress glycogen synthesis, thus favoring lipogenesis vitellogenesis. In Ae. aegypti, roughly one-third of the
to some degree of obesity (Van Handel 1965, Lea and human blood protein is utilized for synthesis of yolk
Van Handel 1970). The amount of sugar ingested before protein, while two-thirds are deaminated and split equally
a blood meal and the extent of subsequent reserve build- for renewed lipid synthesis and for energy requirements.
up are detrimental for the survival of the females (Figure Ziegler and Ibrahim (2001) found a remarkable mechanism
3). Sugar solutions provided in various concentrations in which after a blood meal, yolk lipid is taken from the
clearly affect the survival of a population. As will be pre-blood meal lipid stores in the fat body, while the
shown later, the amount of lipids accumulated until the lipid synthesized from the blood protein is deposited
time of a blood meal largely contributes to the into the fat body for the next gonotrophic cycle. In
reproductive potential of a female mosquito. Selected addition, we had found evidence for a threshold of one
examples shall demonstrate the metabolic strategies calorie for the female lipid content plus the blood meal
 4 Journal of Vector Ecology June, 2003

Figure 2. Teneral protein (P) and lipid (L) of four mosquito species, measured shortly after eclosion and plotted
against body size. All possible body sizes measured as wing length (mm) and presented as cubic value (WL3) were
produced by manipulating larval densities and food supplies. Only the regression lines are shown. The small
hatched segment represents the minimal amounts of lipid observed when females were starved to death, thus
indicating the extent of lipids available for mobilization under extreme nutritive stress. (Data from Briegel 1990a, b;
Briegel et al. 2001; and unpublished data).

Figure 3. Effect of increasing concentrations of dietary

sugar solutions on female survival for large and small
Ae. aegypti and An. gambiae. The 50% (solid lines) and
maximal (dashed lines) survival times are depicted as
regressions, based on earlier data (Briegel et al. 2001a, b,
and unpublished data). Survival under starvation, i.e.
access to water only, is shown by gray shading for the
cohorts tested.
June, 2003 Journal of Vector Ecology 5

females became physiologically older, the more they

withheld the lipid in their fat body instead of transferring
it into oocytes. This surprising result provides an
explanation for the steadily declining fecundity in older
females; they become “fat old ladies.” The physiological
alterations within the fat body should be investigated to
fully understand this “selfish” behavior of older Ae.
aegypti females. Figure 7 also shows the development
of strong flight potentials for Ae. aegypti. After eclosion
it takes 2-3 days of sugar-feeding for females to reach
their strongest flight potentials of >5000 m/night in 50%
of the cohort.
Ae. vexans, a major nuisance in the holarctic region
and known for its migratory flights (Clements 1999), is a
different case. It is of larger size but considerably lower
Figure 4. Temporal sequence of physiological processes in teneral protein and lipids (Briegel et al. 2001a, Figure
during one gonotrophic cycle of Ae. aegypti, all values 2). How does it cope with its poor teneral reserve status?
expressed as a percent of their respective maxima. 1: During the first week of imaginal life, female Ae. vexans
intestinal amino peptidase activity; 2: intestinal trypsin must feed on sugar or otherwise die within 4-6 days.
activity; 3: yolk volume (dots and line); the shaded area They can multiply their teneral lipid roughly 10 times
comprises uric acid and urea excretion, yolk protein and during the first week, and up to 20 times during the
yolk lipid deposition into oocytes; 4: hematin defecation; second week (Figure 8). Once the lipids have been
5: yolk glycogen deposition into oocytes. Arginase increased during their first week, females seek blood
activity in the fat body closely follows the course of meals. After 5-6 d, up to 100-120 eggs may be matured
intestinal trypsin activity, and xanthin dehydrogenase per female. Before that, they generally do not take blood
(XDH), also localized in the fat body, parrallels intestinal meals, but if these were forced, egg maturation failed. At
leucine amino peptidase activity, both not shown for the same time, we recorded the flight potentials of
reasons of clarity. Arginase has a 10%, and XDH a 40% individual mosquitoes. Their reserves are routinely
residual activity, because these two enzymes are active analyzed before and after flights and compared to fixed-
throughout life. (Data adopted from our earlier wing controls kept 20 h motion-less. The data from such
publications). flight protocols (Figure 9 as one example) reveal the total
flight distances in km, and the temporal pattern of flight
activities. Non-stop flight segments of several hours are
protein to be ingested, critical for initiation of oogenesis, regularly observed, interrupted by periods of inactivity
and not just the amounts of blood meal intake (Briegel, that we assume represent phases of reserve mobilizations
unpublished data). Together, these observations explain from the abdominal fat body, the primary storage site, to
that the teneral and/or sugar-derived lipid (Figure 7, the flight muscles. The flight potential is marginal during
bottom) is relevant for the reproductive processes once the first few days, but it develops from the second week
protein has been ingested. This also explains why small onwards. Flights of up to 17 km within one night become
females are unable to mature a batch of eggs with their possible, indicating typical migratory behavior (Figure
first blood meal on teneral reserves alone. When sugar- 8). During such strong flights, up to 50% of the glycogen
fed females obtained rat blood however, fecundity was reserves are utilized together with a 7% disappearance
doubled as a consequence of non-limiting isoleucine of the lipids.
contents in rodent blood (Briegel 1985). Furthermore, In conclusion, two phases are clearly recognized in
there were reversed proportions between uric acid and this species: first fill up the fat body with lipids, for which
urea excretion, depending on whether females had access no long flights are required, while at the same time the
to water (Figure 6: d versus w). In the three Anopheles reproductive system requires a maturation period of
species tested, however, yolk protein always remained similar duration as the flight muscles. Only afterwards,
below 20% of the blood meal protein. hunger for the missing protein develops and blood
To investigate the significance of the lipid reserves donors need to be found by migrations over long
of sugar-fed female Ae. aegypti, we recently followed distances. Indeed, females attacking us in the field always
the lipid metabolism through 5-6 gonotrophic cycles in carry remarkable lipid reserves that are considerably
large and small females (Briegel et al. 2002). As the above their teneral values. Similar strategies were
 6 Journal of Vector Ecology June, 2003

described by Renshaw et al. (1995) for Oc. cantans which

resembles the Ae. vexans type, and were also found in
Ae. triseriatus (Briegel unpublished data) and Ae.
albopictus (Briegel and Timmermann 2001), as well as in
Oc. punctor (Renshaw et al. (1995), the latter three
resembling Ae. aegypti.
Still another situation is encountered in the
Anophelini. As mentioned before, these are surface
feeders and the air-water interface is of lower nutritional
value than the bottom of a puddle with all its organic
matter. An. gambiae has a smaller body size, and An.
albimanus is similar to or even larger than Ae. aegypti,
but because in both Anopheles species, protein and lipid
follow isometric relationships, although on a much lower
level, they might be called “skinny” (Briegel 1990b).
Tropical Anopheles have evolved the following strategies
and adaptations. First of all, they can successfully feed
on blood donors within half a day of eclosion (Figure 7),
often without extended sugar feeding. Indeed, their
lipogenetic capabilities are lower than in Culicini. But
appreciable flight potentials soon develop (Figure 7).
Second, the blood meal protein is concentrated during
feeding, comparable to aphids with their water (and
sugar) removal, which in turn requires extended feeding
times (Briegel and Rezzonico 1985) and is in line with
their preference for biting at night when hosts are less
active and less sensitive. This behavior allows blood
meal volumes of up to 10-12 µl (or mg), as compared to
usually 2-5 µl in Aedes. In addition, An. albimanus express
a considerable constitutive trypsin activity in their midgut
shortly after eclosion, which allows immediate digestion
after blood ingestion, well before the inductive trypsin
is synthesized a few hours later. Third, multiple blood
meals can be taken at short intervals, even within a single
night, occasionally leading to a daily oviposition rhythm
(Hörler and Briegel 1995).
Furthermore, in An. albimanus, which are smaller
than 3 mm wing length, the first blood meal is used for
the synthesis of maternal lipid and protein reserves, and
not for yolk, thus compensating for their low teneral
amounts (Briegel 1990a). Synthesis of yolk components
in such instances is achieved from subsequent blood
Figure 5. Demonstration of synchronous synthesis of meals, but the efficiency of blood protein utilization for
yolk protein and yolk lipid (A), parallel to increasing yolk synthesis always remains <10% of the caloric input,
yolk volumes (B); uric acid is synthesized in synchrony much lower than in Culicini. In spite of these metabolic
with urea formation (C), and both are synchronous with constraints, total fecundity of An. albimanus with 200-
yolk protein and lipid deposition (compare Figure 3). 400 eggs per female within the first week of its imaginal
Only glycogen synthesis occurs much later. The life with daily blood meals is roughly equal, if not higher
discontinuity of yolk protein and lipid formation at than the fecundity of about 290 eggs per female in Ae.
volumes of 90% (B) is caused by the elongation of the aegypti during the same period.
oocytes observed between 30-36 hr after blood meal (from Thus, I think the concept of gonotrophic cycles is
Briegel et al. 2003). questionable for Anopheles species. It appears that more
or less rigid gonotrophic cycles may have evolved
June, 2003 Journal of Vector Ecology 7

Figure 6. Nitrogen partitioning during a gonotrophic cycle of four mosquito species fed human blood (h). All
females had access to sucrose before the blood meal. Ae. aegypti was also fed rodent blood (r), and furthermore
were kept in dryness (d) or with access to drinking water (w). The black segments are for haematin which always
accounts for 2-3%. Note the variable protein input by blood meal, caused by the body sizes and midgut volumes of
the different Anopheles species; in Ae. aegypti blood meals were given by enema. The average number of eggs
matured for each condition is added at the bottom of each bar. The segment with vertical shading represents the
maternal, extraovarian protein deposit, synthesized from the blood meal before and/or together with the yolk
protein. Further explanations see text. Abbreviations: Y for yolk, UA for uric acid, UR for urea, AM for ammonium
plus amino nitrogen (combined). In An. gambiae the budget was not completed.

Figure 7. Comparison of reserve synthesis, feeding

attempts and success, and flight performances between
female Ae. aegypti and An. gambiae. For the synthesis
of glycogen and lipid (bottom panel) the caloric values
are expressed as multiples of the respective teneral
values, that arbitrarily are given as 1. The feeding activity
develops within 1 day of eclosion in both species (top
panel), but successful oogenesis is delayed in An.
gambiae (indicated by black segments within the circles).
Flight performance in Ae. aegypti revealed two clearly
visible segments: strong fliers (i.e. >5 km per night, dark
shading) were encountered already by day 3 (over 50%),
whereas the majority of the remaining females were
average fliers (i.e. 1000-5000 m/night); the smallest
segments were poor fliers. An gambiae are mostly average
fliers; only at days 4, 5, 8, and 14 some very strong fliers
(>5000m/night; 10-20%) were observed with up to 17
km/night.
 8 Journal of Vector Ecology June, 2003

Figure 9. Two examples of flight mill protocols of 3-day-

old female Ae. aegypti with access to water (top) or sugar
(bottom). The total flight distances flown during 16 hr
were 0.9±0.8 km (N=14) and 5.7±3.0 km (N=16) per female,
respectively.

predominately in the Culicini. If true, this suggestion

bears considerable consequences for the hormonal
regulations that have been established for Aedes or
Culex (Lea 1975). The hormones might be the same ones
among the two tribes (M.R. Brown, personal
communication), but no cyclicity has to be maintained in
the Anophelini.
Another interesting aspect was encountered during
our flight studies with An. gambiae (Figure 7) or An.
albimanus, both strong fliers. We always found
Figure 8. Feeding (top), flying (center), and reserve substantial reductions of their pre-blood meal lipid
synthesis (bottom) in Ae. vexans, showing a different contents during the flight periods. The metabolic basis
timing and extent of these events and therefore different for lipid oxidation by flight muscles unfortunately has
strategies than in the other two species of the foregoing not been investigated in these insects. An alternative
Figure. Note the tremendous amounts of reserves built possibility would be to test for proline oxidation, which
up during the first two weeks of imaginal life (bottom depends on the lipid reserves, as was found earlier for
panel). Feeding success followed by oogenesis requires Glossina (Bursell et al. 1974, Langley 1977).
roughly one week of development (top panel). Flight For pathogen-carrying females, such as those
performances also develop slowly and gradually. Strong infected with Plasmodium, our results bear
fliers (dark shading) reached up to 17 km per single night epidemiological consequences, that suggest much
on the flight mill, but only after several days. In the top higher vector potentials than assumed so far. To fully
panel, triangles are for females that had access to water ascertain such epidemiological consequences in
from eclosion, circles for sugar-fed females; the extent of Anopheles, experiments should be extended for at least
black indicates 50% or 100% oogenesis in these female the duration of the extrinsic incubation time of
cohorts. Plasmodium.
June, 2003 Journal of Vector Ecology 9

We are considering an evolutionary interpretation remains an endless future for the field of basic
that the physiological and endocrine principles physiology.
governing the discrete gonotrophic cycles in Culicines
have evolved later, representing an apomorph status. I Acknowledgments
even dare to think that the possibility for acyclic
reproduction in tropical Anopheles as a plesiomorph I would like to thank all the brilliant students who
status might contribute to or explain the fact that passed through my laboratory as highly motivated
Plasmodium has adopted Anophelini as their vectors, biologists. The most important and productive
and not the Culicini. contributions and discussions were with R. Graf, E. Hörler,
In conclusion, I would like to convey a few personal and S.E. Timmermann, to name just a few. Much of my
remarks. Some entomologists have objected to issues own work largely depended on the competent and
raised from our physiological laboratory investigations reliable laboratory technicians, E. Csibi and R. Haigis.
versus ecological and epidemiological field studies. I The most substantial part, however, was played by Arden
never claimed that our laboratory-based results with O. Lea, who continuously asked stimulating questions
controlled and constant conditions would represent the before and after experiments. As a post-doc in his highly
actual life of a given vector in its natural environment, scientific and unusually creative surroundings, I received
and I am aware of many additional parameters in the the best training I could ever have had. Equally important
field that equally govern mosquito ecology. What I have was the absolute freedom of research I was always
always tried to provide, however, was a valid and largely granted by the director of our institute, Prof. R. Wehner.
quantitative background, and to present a framework Finally, the continuous and generous support of our
against which ecologists could seek additional research during 26 years by the Swiss National Science
possibilities or interpretations of their findings. In the Foundation is greatly appreciated.
laboratory I think we could stretch that frame to the
extremes, while other parameters were kept constant, to REFERENCES CITED
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