Sweet waste extract uptake by a mosquito vector: Survival, biting, fecundity responses, and potential epidemiological significance

Abstract

In nature, adult mosquitoes typically utilize nectar as their main energy source, but they can switch to
other as yet unidentified sugary fluids. Contemporary lifestyles, with their associated unwillingness to
consume leftovers and improper disposal of waste, have resulted in the disposal of huge amounts of waste
into the environment. Such refuse often contains unfinished food items, many of which contain sugar
and some of which can collect water from rain and generate juices. Despite evidence that mosquitoes
can feed on sugar-rich suspensions, semi-liquids, and decaying fruits, which can be abundant in garbage
sites, the impacts of sweet waste fluids on dengue vectors are unknown. Here, we investigated the effects
of extracts from some familiar sweet home waste items on key components of vectorial capacity of
Aedes aegypti. Adult mosquitoes were fed one of five diets in this study: water (WAT); sucrose (SUG);
bakery product (remnant of chocolate cake, BAK); dairy product (yogurt, YOG); and fruit (banana (BAN).
Differences in survival, response time to host, and egg production were examined between groups. For
both males and females, maintenance on BAK extract resulted in marked survival levels that were similar
to those seen with SUG. Sweet waste extracts provided better substrates for survival compared to water,
but this superiority was mostly seen with BAK. Females maintained on BAK, YOG, and BAN exhibited
shorter response times to a host compared to their counterparts maintained on SUG. The levels of egg
production were equivalentin waste extract- and SUG-fed females. The findings presented here illustrate
the potential of sweet waste-derived fluids to contribute to the vectorial capacity of dengue vectors and
suggest the necessity of readdressing the issue of waste disposal, especially that of unfinished sweet
foods. Such approaches can be particularly relevant in dengue endemic areas where rainfall is frequent
and waste collection infrequent.

Full text

Acta
Tropica
169
(2017)
84–92
Contents
lists
available
at
ScienceDirect
Acta
Tropica
jo
u
r
n
al
homep
age:
www.elsevier.com/locate/actatropica
Sweet
waste
extract
uptake
by
a
mosquito
vector:
Survival,
biting,
fecundity
responses,
and
potential
epidemiological
significance
Hamady
Dienga,∗,
Tomomitsu
Sathob,
Fatimah
Abangc,
Nur
Khairatun
Khadijah
Binti
Melic,
Idris
A.
Ghanid,
Cirilo
Nolasco-Hipolitoc,
Hafijah
Hakimd,
Fumio
Miakeb,
Abu
Hassan
Ahmade,
Sabina
Noorc,
Wan
Fatma
Zuharahe
,
Hamdan
Ahmade,
Abdul
Hafiz
A.
Majide,
Ronald
E.
Morales
Vargasf,
Noppawan
P.
Moralesg,
Siriluck
Attrapadungf,
Gabriel
Tonga
Nowega
aInstitute
of
Biodiversity
and
Environmental
Conservation
(IBEC),
Universiti
Malaysia
Sarawak,
Kuching,
Kota
Samarahan,
Malaysia
bFaculty
of
Pharmaceutical
Sciences,
Fukuoka
University,
Japan
cFaculty
of
Resource
Science
and
Technology,
Universiti
Malaysia
Sarawak,
Kota
Samarahan,
Malaysia
dFaculty
of
Science
and
Technology,
Universiti
Kebangsaan
Malaysia,
Bangi,
Malaysia
eSchool
of
Biological
Sciences,
Universiti
Sains
Malaysia,
Penang,
Malaysia
fFaculty
of
Tropical
Medicine,
Mahidol
University,
Thailand
gFaculty
of
Science,
Mahidol
University,
Thailand
a
r
t
i
c
l
e
i
n
f
o
Article
history:
Received
8
December
2016
Received
in
revised
form
17
January
2017
Accepted
17
January
2017
Available
online
4
February
2017
Keywords:
Aedes
aegypti
Sweet
waste
Survival
Responsiveness
to
host
Fecundity
a
b
s
t
r
a
c
t
In
nature,
adult
mosquitoes
typically
utilize
nectar
as
their
main
energy
source,
but
they
can
switch
to
other
as
yet
unidentified
sugary
fluids.
Contemporary
lifestyles,
with
their
associated
unwillingness
to
consume
leftovers
and
improper
disposal
of
waste,
have
resulted
in
the
disposal
of
huge
amounts
of
waste
into
the
environment.
Such
refuse
often
contains
unfinished
food
items,
many
of
which
contain
sugar
and
some
of
which
can
collect
water
from
rain
and
generate
juices.
Despite
evidence
that
mosquitoes
can
feed
on
sugar-rich
suspensions,
semi-liquids,
and
decaying
fruits,
which
can
be
abundant
in
garbage
sites,
the
impacts
of
sweet
waste
fluids
on
dengue
vectors
are
unknown.
Here,
we
investigated
the
effects
of
extracts
from
some
familiar
sweet
home
waste
items
on
key
components
of
vectorial
capacity
of
Aedes
aegypti.
Adult
mosquitoes
were
fed
one
of
five
diets
in
this
study:
water
(WAT);
sucrose
(SUG);
bakery
product
(remnant
of
chocolate
cake,
BAK);
dairy
product
(yogurt,
YOG);
and
fruit
(banana
(BAN).
Differences
in
survival,
response
time
to
host,
and
egg
production
were
examined
between
groups.
For
both
males
and
females,
maintenance
on
BAK
extract
resulted
in
marked
survival
levels
that
were
similar
to
those
seen
with
SUG.
Sweet
waste
extracts
provided
better
substrates
for
survival
compared
to
water,
but
this
superiority
was
mostly
seen
with
BAK.
Females
maintained
on
BAK,
YOG,
and
BAN
exhibited
shorter
response
times
to
a
host
compared
to
their
counterparts
maintained
on
SUG.
The
levels
of
egg
production
were
equivalent
in
waste
extract-
and
SUG-fed
females.
The
findings
presented
here
illustrate
the
potential
of
sweet
waste-derived
fluids
to
contribute
to
the
vectorial
capacity
of
dengue
vectors
and
suggest
the
necessity
of
readdressing
the
issue
of
waste
disposal,
especially
that
of
unfinished
sweet
foods.
Such
approaches
can
be
particularly
relevant
in
dengue
endemic
areas
where
rainfall
is
frequent
and
waste
collection
infrequent.
©
2017
Elsevier
B.V.
All
rights
reserved.
∗Corresponding
author
at:
Institute
of
Biodiversity
and
Environmental
Conser-
vation,
Faculty
of
Resource
Science
and
Technology,
Universiti
Malaysia
Sarawak,
Kota
Samarahan,
Malaysia.
E-mail
address:
hamachan1@yahoo.com
(H.
Dieng).
1.
Introduction
Several
outbreaks
of
dengue
and
related
diseases,
such
as
Zika
fever,
have
been
reported
in
recent
years,
mostly
from
urban
cen-
ters,
with
smaller
numbers
of
cases
from
rural
areas
(Banerjee
et
al.,
2015).
Urbanization
and
globalization
have
led
to
overcrowding
of
cities
(Kang,
2014).
Urban
centers
are
also
characterized
by
the
gradual
replacement
of
traditional
foods
by
processed
and
ready-
made
foods
(Hurtig,
2009),
excessive
purchasing,
over-preparation
http://dx.doi.org/10.1016/j.actatropica.2017.01.022
0001-706X/©
2017
Elsevier
B.V.
All
rights
reserved.

H.
Dieng
et
al.
/
Acta
Tropica
169
(2017)
84–92
85
and
unwillingness
to
consume
leftovers
(Gustavsson
et
al.,
2011),
increased
usage
of
plastic
and
glass
containers
in
various
forms
(Asian
Productivity
Organization
(2007),
improper
disposal
atti-
tudes
(Anomanyo,
2004;
Da
et
al.,
2008),
insufficient
disposal
facilities
(Gregory
et
al.,
1996),
and
inadequate
waste
management
(Jacobi
and
Besen,
2011).
These
attitudes
and
management
issues
have
resulted
in
huge
amounts
of
household
waste
being
discarded
into
the
environment
(Banerjee
et
al.,
2015).
Leftover
food
items,
packaging
(Gustavsson
et
al.,
2011;
Jacobi
and
Besen,
2011),
and
containers
made
of
plastic
or
glass
constitute
the
bulk
of
household
waste
(Banerjee
et
al.,
2015).
Dengue
vectors
typically
thrive
in
artificial
container
habitats
(Higa,
2011)
and
can
colonize
any
container
flooded
by
rainfall
(Liehne,
1988;
Juliano
et
al.,
2002).
When
glass
and
plastic
contain-
ers
are
discarded,
they
can
retain
rainwater,
and
become
potential
breeding
sites
for
container-inhabiting
Aedes
mosquitoes
(Barrera
et
al.,
1993).
Over
26
types
of
waste
containers
have
been
found
positive
for
immature
stages
of
Aedes
(Banerjee
et
al.,
2013,
2015).
In
addition
to
providing
breeding
habitats,
discarded
household
products
can
contain
nutrients
in
readily
available
quantities.
Glob-
ally,
around
one
third
of
the
edible
parts
of
food
produced
for
human
consumption
are
discarded
as
waste
(UN/FAO,
2011).
In
industrialized
Asia,
food
waste
per
person
per
year
is
around
80
kg
(Gustavsson
et
al.,
2011).
Malaysians
throw
away
9000–15000
t
of
unfinished
food
daily
(Nation,
2016).
In
urban
areas
where
rainfall
is
frequent
and
waste
collection
infrequent,
sweet
waste
can
have
an
important
impact
on
the
mosquito
community
and
significant
epidemiological
implications.
There
is
evidence
that
food
waste
contains
many
sweet
products:
bakery
(cakes
and
desserts),
parts
of
fruits
(bananas,
apples,
pineapples,
plums,
peaches),
canned
drinks,
dairy
products
(yogurt),
and
jams
(WRAP,
2009).
In
situations
sim-
ilar
to
those
reported
by
WRAP
(2009),
juicy,
sweet,
and
fragrant
fruits,
such
breadnuts,
durians,
breadfruits,
and
jackfruits,
are
com-
monly
observed
discarded
in
Malaysia.
In
a
garbage
survey
carried
out
in
2016
in
Kota
Samarahan,
partly
eaten
apples
and
Kit
Kat
chocolate
bars
were
found
in
some
garbage
sites
near
residences.
The
sugar
contents
of
the
foods
used
in
homes
that
are
later
discarded
uneaten
is
diverse
and
appreciable.
For
example,
some
sweet
beverages
contain
sweeteners,
such
as
sucrose
(50%
glucose,
50%
fructose),
high-fructose
corn
syrup
(HFCS;
most
often
45%
glu-
cose
and
55%
fructose),
or
fruit
juice
concentrates
(Malick
and
Hu,
2012).
A
can
of
cola
contains
33
g
of
sugar
(Brown,
2016).
Syrups
(67%
granulated
sugar
dissolved
in
water)
are
commonly
used
in
a
range
of
baked
goods
and
confectionery
(British
Sugar,
2012).
One
hundred
grams
of
pineapple,
apple,
or
banana
contains
9.9,
10.4,
and
12.2
g
of
sugar,
respectively
(NAL
USDA,
2016).
Fructose
occurs
naturally
in
fruits
(Park
and
Yetley,
1993)
and
apple
juice
contains
high
concentrations
of
free
fructose
(Riby
et
al.,
1993).
Glu-
cose
occurs
in
fruits
and
its
syrup
is
widely
used
in
the
manufacture
of
foodstuffs
(Ushijima
et
al.,
1991).
Sucrose
is
found
in
some
fruits
and
some
roots,
e.g.,
carrot
(Buss
and
Robertson,
1976),
and
lactose
is
found
primarily
in
many
dairy
products
(Kimball,
2012).
Fructose,
glucose,
sucrose,
starch,
and
a
few
unknown
sugars
have
been
found
in
wild
female
mosquitoes
(Burkett
et
al.,
1998).
In
fact,
sugar
is
a
staple
of
mosquitoes
(Gary
and
Foster,
2004),
as
illus-
trated
by
behavioral,
structural,
and
physiological
specializations
for
finding,
feeding
on,
and
assimilating
it
in
both
sexes
(Foster,
1995).
In
the
wild,
finding
a
suitable
sugar
meal
is
one
of
the
most
critical
challenges
faced
by
mosquitoes
(Gary
and
Foster,
2004;
Clements,
1992).
An
adequate
dietary
sugar
supply
is
a
critical
aspect
of
survival
(Burkett
et
al.,
1998),
longevity,
and
popula-
tion
maintenance
(Thorsteinson
and
Brust,
1962).
Energy
gained
from
sugar
intake
is
necessary
to
maintain
male
sexual
perfor-
mance
(Clements,
1955;
Nayar
and
Van
Handel,
1971)
and
female
vectorial
capacity
(Gouagna
et
al.,
2010;
Gu
et
al.,
2011).
Sugar-
fed
females
show
enhanced
survival,
host-finding
ability
(Foster
and
Eischen,
1987;
Walker
and
Edman,
1985),
and
increased
possi-
bility
of
vectoring
pathogens
than
those
that
have
been
starved
or
fed
on
water
(Kelly
and
Edman,
1996;
Burkett
et
al.,
1998).
Sugar-deprived
males
or
females
typically
die
within
a
few
days
(Foster,
1995).
Ingested
sugars
increase
flight
activity
and
range
for
mosquitoes
of
both
sexes,
(Abraham,
2013).
Male
mosquitoes
rely
mostly
on
sugar-rich
diets
to
engage
in
the
energetically
costly
swarming
(Kaufmann
et
al.,
2013)
and
gamete
production
(Foster,
1995).
Some
mosquitoes
do
not
seek
blood
until
they
take
at
least
one
sugar
meal
(Renshaw
et
al.,
1994;
Briegel
et
al.,
2001).
A
sugar
meal
is
necessary
to
initiate
the
development
of
ovarian
folli-
cles
(Abraham,
2013)
and
the
first
batch
of
eggs
(O’Meara,
1985).
The
occurrence
of
sugar
feeding
during
an
ovarian
cycle
promotes
the
rate
of
egg
development
(Nayar
and
Sauerman,
1975).
Sugar
feeding
also
influences
offspring
quality
through
a
maternal
effect
(Fernandes
and
Briegel,
2005).
The
deprivation
of
sugar
after
com-
pletion
of
egg
development
results
in
eggs
with
depleted
glycogen
deposits
(van
Handel,
1992).
Without
sugar,
mosquitoes
can
die
rapidly,
despite
frequent
access
to
blood
(Nayar
and
Sauerman,
1971;
Fernandes
and
Briegel,
2005).
In
the
laboratory,
it
is
stan-
dard
practice
to
provide
mosquito
colonies
with
a
variety
of
sugar
solutions,
and
female
Ae.
aegypti
mosquitoes
lived
much
longer
in
the
laboratory
when
fed
with
both
sugar
and
blood
than
when
fed
with
blood
alone
(Clements,
1992).
In
fact,
such
practices
mimic
the
availability
of
natural
sugars
in
the
wild
(Gillett
et
al.,
1962;
Gouagna
et
al.,
2010).
To
supplement
their
energy
reserves
and
sustain
life
in
nature,
both
sexes
feed
almost
exclusively
on
plant-derived
sugary
fluids,
including
sap,
nectar,
honeydew,
and
fruits
(Clements,
1992;
Foster,
1995;
Foster
and
Takken,
2004).
There
is
evidence
that
mosquito
populations
prevail
mostly
in
environments
where
sugar
resources
are
available.
Gu
et
al.
(2011)
found
a
250-fold
difference
in
the
malarial
vectorial
capacity
between
sugar
resource-rich
and
sugar-
poor
sites,
where
the
vector
could
not
maintain
a
viable
population.
Despite
immense
diversity
of
flowering
plants
that
can
serve
a
priori
as
sugar
sources
(Gouagna
et
al.,
2010),
it
has
been
reported
that
mosquitoes
do
not
acquire
sugar
meals
from
all
flowering
plants
(Müller
and
Schlein,
2005).
Ae.
aegypti
and
other
aedines
were
reported
to
feed
on
only
three
of
24
native
plant
species
offered
to
them
in
Canada
(Abdel-Malek
and
Baldwin,
1961).
In
the
absence
of
favorable
sugar
sources,
mosquitoes
can
switch
to
other
sources
(Müller
and
Schlein,
2005).
There
is
evidence
that
mosquitoes
can
feed
on
sugar-rich
sticky
suspensions
(Abraham,
2013),
semi-
liquids
(Eliason,
1963),
dry
food
(Downs
and
Arizmendi,
1951),
healthy
plant
tissues
(Schlein
and
Müller,
1995),
and
damaged
or
decaying
fruits
(Foster,
1995).
Although
confirmed
to
be
of
plant
origin
(Gary
and
Foster,
2004;
Gouagna
et
al.,
2010),
the
actual
sources
of
sugary
fluids
upon
which
mosquitoes
feed
in
nature
are
still
unknown
(Gouagna
et
al.,
2010).
Thus,
further
studies
are
needed
to
identify
the
cryptic
sources
of
sugar
of
wild
mosquitoes.
Although
some
household
wastes
have
been
reported
to
act
as
larval
development
sites
for
dengue
vectors
(Banerjee
et
al.,
2013)
and
another
study
addressed
their
seasonal
productivity
relative
to
urbanization
level
(Banerjee
et
al.,
2015),
there
have
been
no
studies
regarding
the
potential
of
discarded
household
products
as
sources
of
energy
for
adult
dengue
mosquitoes.
Here,
we
evaluated
the
capacity
of
the
extracts
of
some
common
sweet
home
wastes
on
key
components
of
the
vectorial
capacity
of
Ae.
aegypti.
2.
Materials
and
methods
2.1.
Ethical
statement
This
study
was
approved
by
the
Biological
Research
Ethics
Com-
mittee
at
University
Malaysia
Sarawak
(UNIMAS).

86
H.
Dieng
et
al.
/
Acta
Tropica
169
(2017)
84–92
2.2.
Mosquito
rearing
and
stocks
Ae.
aegypti
was
used
in
this
study.
A
sub-colony
was
produced
from
a
colony
maintained
under
controlled
conditions
(27 ◦C–30 ◦C,
RH
60%–86%,
photoperiod
of
14:10
h
(L:D))
at
the
Entomology
Unit
of
the
Faculty
of
Resource
Science
and
Technology
(Univer-
siti
Malaysia
Sarawak,
Kota
Samarahan,
Sarawak,
Malaysia).
Larvae
were
routinely
reared
in
plastic
trays
(As
One
Corporation,
Osaka,
Japan)
containing
1
L
of
tap
water
as
reported
previously
(Gary
and
Foster,
2001)
and
fed
a
diet
of
cat
food
pellets
(ProDiet
Cat
Food,
Malaysia).
Adults
were
kept
in
rearing
cages
(30
×
30
×
30
cm,
Bug-
Dorm;
MegaView
Science
Co.,
Ltd.,
Taichung,
Taiwan)
and
provided
10%
sucrose
solution.
Pupae
were
collected
into
250-mL
plastic
con-
tainers
containing
10
mL
of
water
and
transferred
to
rearing
cages
(30
×
30
×
30
cm,
BugDorm;
MegaView
Science
Co.,
Ltd.).
Emerg-
ing
adults
were
continuously
provided
with
10%
sucrose
solution.
Four
days
after
emergence,
females
were
given
blood
meals
on
restrained
hamsters.
Three
days
after
blood
feeding,
plastic
vials
(2
cm
wide
and
8
cm
deep)
containing
a
piece
of
filter
paper
as
an
oviposition
substrate
were
placed
inside
cages
for
egg
collection.
Eggs
were
dried
under
room
four
days
later
at
room
temperature
for
4
days
in
the
laboratory
and
kept
as
stock
colony.
2.3.
Experimental
food
products
and
tested
experimental
diets
Five
diets
were
tested
in
this
study:
water,
sugar
(sucrose),
a
bak-
ery
product
(cake),
a
dairy
product
(yogurt),
and
a
fruit
(banana).
Sugar
is
a
staple
food
of
mosquitoes,
and
both
sexes
must
feed
daily
on
it
as
the
main
energy
source
for
longevity,
fecundity,
host
seek-
ing,
blood
feeding,
and
disease
transmission
(Yuval,
1992;
Gary
and
Foster,
2004).
In
general,
fruits,
bakery,
and
dairy
products
are
rich
in
sugar
and
often
served
as
desserts
after
the
main
dish.
People
often
do
not
eat
an
entire
dessert,
for
which
the
useful
life
is
rela-
tively
short.
Most
dessert
products
remain
unfinished
and
end
up
as
waste.
Therefore,
we
used
partly
eaten
moist
chocolate
cake
(Secret
Recipe
Cakes
&
Café
Sdn
Bhd,
Kuala
Lumpur,
Malaysia),
yogurt
(Yoplait
Mixed
Berry
yogurt),
and
Borneo
banana
strain
(Pisang
Madu,
which
means
honey
banana)
as
experimental
sweet
waste
products.
Remnants
of
chocolate
cake,
yogurt,
and
banana
were
obtained
from
volunteers.
For
each
of
these
food
remnants
and
sugar,
four
replicates
of
5
g
of
smashed
matter
were
each
soaked
in
100
mL
of
water
in
250-mL
plastic
containers.
After
soaking
for
5
min,
the
soups
were
stirred
using
spoons.
After
3
min
of
stirring,
the
different
brews
were
filtered
using
a
60-wire
mesh.
For
conve-
nience,
the
four
solutions
obtained
from
sugar,
bakery,
yogurt,
and
banana
after
filtration
were
referred
to
as
5%
sucrose
solution
(SUG),
5%
BAK
extract
(BAK),
5%
YOG
extract
(YOG),
and
5%
BAN
extract
(BAN).
SUG
was
used
as
a
positive
control,
and
water
(WAT)
served
as
a
negative
control
(Table
1).
2.4.
Experimental
mosquitoes
Newly
emerged
males
and
females
(NEMs
and
NEFs)
derived
from
larvae
reared
at
a
density
of
150/L
of
water
and
fed
0.5
g
of
powdered
cat
food
pellets
were
provided
with
10%
sucrose
solution
for
3
days
and
later
had
continuous
access
to
SUG
and
were
con-
sidered
as
SUG-fed
males
and
SUG-fed
females,
respectively.
NEMs
and
NEFs
fed
10%
sucrose
solution
for
3
or
4
days
and
then
given
continuous
access
to
BAK
were
used
as
BAK-fed
males
and
BAK-fed
females,
respectively.
NEMs
and
NEFs
provided
with
10%
sucrose
solution
for
3
or
4
days
and
then
maintained
on
YOG
served
as
YOG-fed
males
and
YOG-fed
females,
respectively.
NEMs
and
NEFs
provided
with
10%
sucrose
solution
for
3
or
4
days
and
then
kept
on
BAN
extract
were
used
as
BAN-fed
males
and
BAN-fed
females,
respectively.
NEMs
and
NEFs
provided
with
10%
sucrose
solution
Table
1
Making
of
experimental
adult
diets.
Food
Operations
Diet
Sugar
5
g
of
sucrose
in
100
mL
of
cool
boiled
water,
and
permitted
to
fully
dissolve
Sucrose
solution
(5%)
(SUG)
Partly
eaten
chocolate
cake
5
g
of
cake
in
100
mL
of
cool
boiled
water;
3-min
stirring;
solution
filtered
using
a
fine
mesh
mosquito
netting
Bakery
(5%)
(BAK)
Partly
eaten
yogurt 5
g
of
yogurt
in
100
mL
of
cool
boiled
water;
3-min
stirring;
solution
filtered
using
a
fine
mesh
mosquito
netting
Yoghurt
(5%)
(YOG)
Partly
eaten
banana
5
g
of
banana
flesh
in
100
mL
of
cool
boiled
water;
3-min
stirring;
solution
filtered
using
a
fine
mesh
mosquito
netting
Banana
(5%)
(BAN)
Table
2
Production
of
experimental
adults.
Rearing
conditions
Adult
type
Newly
emerged
males
(NEMs)
Kept
on
10%
sucrose
solution
(SS)
for
3
days
then
continuously
kept
on
5%
SS
SUG-fed
males
NE
females
(NEFs)
Kept
on
10%
SS
for
4
days
then
continuously
kept
on
5%
SS
SUG-fed
females
NEMs
Kept
on
10%
SS
for
3
days
then
continuously
kept
on
BAK
extract
BAK-fed
males
NEFs
Kept
on
10%
SS
for
4
days
then
continuously
kept
on
BAK
extract
BAK-fed
females
NEMs
Kept
on
10%
SS
for
3
days
then
continuously
kept
on
YOG
extract
YOG-fed
males
NEFs
Kept
on
10%
SS
for
4
days
then
continuously
kept
on
YOG
extract
YOG-fed
females
NEMs
Kept
on
10%
SS
for
3
days
then
continuously
kept
on
BAN
extract
BAN-fed
males
NEFs
Kept
on
10%
SS
for
4
days
then
continuously
kept
on
BAN
extract
BAN-fed
females
NEMs
Kept
on
10%
SS
for
3
days
then
continuously
kept
on
WAT
WAT-fed
males
NEFs
Kept
on
10%
SS
for
4
days
then
continuously
kept
on
WAT
WAT-fed
females
for
3
or
4
days
and
then
placed
on
a
WAT
regime
were
considered
as
WAT-fed
males
and
WAT-fed
females,
respectively
(Table
2).
2.5.
Survival
responses
following
uptake
of
different
types
of
sweet
waste
extract
Eighty
females
and
100
males
that
emerged
within
3
and
4
days,
respectively,
were
placed
in
a
standard
adult
mosquito
breeding
cage
(30
×
30
×
30
cm)
where
they
had
sustained
access
to
10%
sucrose
solution
from
an
apparatus
similar
to
that
used
elsewhere
(Dieng
et
al.,
2015).
After
three
days
of
sugar
feeding,
68
males
were
divided
into
five
groups
of
12
individuals
each.
Each
individual
from
each
group
was
transferred
into
an
experimental
unit
and
assigned
to
one
of
the
following
feeding
regimes:
i)
SUG
(control);
ii)
BAK
extract;
iii)
YOG
extract;
iv)
BAN
extract;
and
v)
WAT.
Similarly,
68
females
were
divided
into
four
lots
of
12
individuals
each.
Females
of
each
lot
were
placed
individually
in
an
experimental
unit.
Twelve
females
were
fed
SUG
and
12
others
were
kept
on
WAT.
The
three
other
lots
of
twelve
females
each
were
divided
into
BAK,
YOG,
and
BAN
groups.
The
bioassays
were
carried
out
under
controlled
labo-
ratory
conditions
(27 ◦C–30 ◦C,
RH
60%–86%,
photoperiod
14:10
h).
All
120
experimental
units
were
checked
daily
for
death
of
adult
mosquitoes
and
any
dead
males
or
females
were
recorded.
Survival
counts
were
made
at
the
end
of
the
7-day
experimental
feeding
period.

H.
Dieng
et
al.
/
Acta
Tropica
169
(2017)
84–92
87
Fig.
1.
Mean
(±SE)
survival
rates
of
Ae.
aegypti
males
(A)
and
females
(B)
when
given
equal
opportunities
to
feed
on
different
diets
for
1
week.
SUG,
sugar;
BAK,
bakery
(cake);
YOG,
yogurt;
BAN,
banana;
WAT,
water.
2.6.
Changes
in
responsiveness
to
hosts
relative
to
feeding
history
A
second
bioassay
was
carried
out
to
assess
the
response
time
of
Ae.
aegypti
fed
different
diets.
The
experimental
biting
unit
(EBU)
consisted
of
a
standard
mosquito
cage
(30
×
30
×
30
cm)
where
a
single
SUG-fed
female
was
starved
for
10
h
and
permitted
to
accli-
matize.
Following
a
10-min
acclimatization
period,
a
restrained
hamster
within
a
wire
mesh
device
was
placed
at
the
middle
of
the
cage.
Immediately
after
hamster
placement,
an
observer
started
recording
the
time
to
first
biting
attempt
within
30
min.
Eleven
extra
replicates
of
the
treatment
(one
EBU
with
a
single
female
+
restrained
hamster)
were
set
up
on
the
same
or
different
days
and
monitored
as
outlined
for
the
first
EBU.
The
same
treat-
ment
and
monitoring
were
also
carried
out
for
BAK-fed,
YOG-fed,
and
BAN-fed
females
with
12
replicates
in
each
case.
All
observa-
tions
were
performed
between
10:00
and
15:00
under
controlled
laboratory
conditions
as
described
in
the
survival
study.
2.7.
Egg
production
by
Ae.
aegypti
following
uptake
of
different
diets
A
third
experiment
was
conducted
to
examine
the
effects
of
female
diet
on
Ae.
aegypti
egg
production.
Females
that
were
maintained
on
the
SUG
regime
were
blood-fed
to
repletion
using
retrained
hamsters.
Six
fully
blood-fed
SUG-maintained
females
were
singly
transferred
into
standard
mosquito
cages
with
access
to
a
10%
sucrose
solution.
Each
of
these
females
was
dissected
on
the
4th
day
post-blood
feeding
and
eggs
were
enumerated
under
a
dissecting
microscope
(ARMS
AR-Z2;
ARMS
SYSTEM
Co.,
Ltd.,
Tokyo,
Japan).
Blood
feeding
and
dissection
procedures
identical
to
those
performed
for
SUG-fed
females
were
also
carried
out
for
BAK-fed,
YOG-fed,
and
BAN-fed
females
(6,
10,
and
5
replicates,
respectively).
2.8.
Data
collection
In
the
survival
experiment,
the
dates
of
death
were
recorded
for
adult
(male
and
female)
replicates
in
control
(SUG
and
WAT)
and
test
diet
groups
(BAK,
YOG,
and
BAN).
This
information
was
used
to
compute
the
survival
rates
on
days
2,
5,
and
7
after
commence-
ment
of
experimental
feeding.
The
survival
rate
was
calculated
as:
the
number
of
males
or
females
that
survived
after
the
time
points
of
maintenance
on
a
given
diet
treatment/the
initial
number
of
individuals
(males
or
females)
×
100.
The
impacts
of
sweet
waste
extract-based
diets
on
both
sexes
were
analyzed
by
comparing
the
mean
survival
rates
of
males
and
females
in
SUG,
WAT,
BAK,
YOG,
and
BAN.
In
the
host
responsiveness
study,
an
attempted
bite
was
recorded
as
reported
elsewhere
(Turley
et
al.,
2009;
Dieng
et
al.,
2015);
briefly,
when
a
female
landed
on
the
restrained
hamster
and
dynamically
attempted
to
probe
its
skin.
The
time
since
placement
of
the
hamster
into
the
EBU
and
attempted
bite
was
noted
for
each
female
replicate
in
each
feeding
regime.
The
mean
values
of
these
periods
expressed
in
seconds
(s)
were
used
as
measures
of
response
times
to
host.
In
the
egg
production
bioassay,
the
mean
numbers
of
eggs
laid
found
in
the
two
ovaries
of
each
replicate
female
from
each
feeding
regime
were
considered
as
scores
of
egg
production.
2.9.
Statistical
investigations
The
differences
in
survival,
response
time
to
host,
and
egg
pro-
duction
between
SUG
(control)
and
test
diets
were
compared
by
analysis
of
variance
(ANOVA)
using
the
Systat
v.11
statistical
soft-
ware
package
(Systat
Software,
Inc.,
Richmond,
CA,
2004).
Tukey’s
Honest
Significant
Difference
(HSD)
test
was
used
to
dissociate
means.
In
all
analyses,
P
<
0.05
was
taken
to
indicate
statistical
sig-
nificance.
3.
Results
3.1.
Male
survival
patterns
on
different
waste-based
diets
Males
reared
on
SUG
had
a
perfect
survival
(100%)
throughout
the
7-day
observation
period.
In
the
BAK
regime,
there
were
no
significant
temporal
discrepancies
in
survival
rate
(F
=
0.50,
df
=
2,
P
=
0.611).
However,
survival
on
days
5
and
7
(91.66%
±
8.33%,
range
0%–100%)
tended
to
be
lower
compared
to
day
2.
The
YOG
treat-
ment
group
showed
100%
survival
on
day
2
and
decreased
sharply
and
significantly
thereafter
(F
=
60.50,
df
=
2,
P
<
0.001),
reaching
about
8%
on
day
7.
In
the
BAN
treatment
group,
there
were
signifi-
cant
temporal
differences
in
survival
(F
=
68.20,
df
=
2,
P
<
0.001).
All
individuals
survived
on
day
2
after
commencement
of
feeding.
The
survival
rate
decreased
to
83.33%
±
11.33%
on
day
5.
No
males
sur-
vived
on
day
7.
On
WAT,
survival
rate
on
day
2
(58.33%
±
14.86%)
decreased
significantly
on
days
5
and
7
(only
one
individual
was
still
alive
on
day
7)
(F
=
10.28,
df
=
2,
P
<
0.001).
On
day
2,
diet
sig-
nificantly
affected
survival
(F
=
7.85,
df
=
4,
P
<
0.001).
The
survival
rate
on
WAT
was
significantly
lower
than
those
on
SUG
[Matrix
of
pairwise
mean
differences
(MPMD
=
−41.667,
P
<
0.001)]
and
waste

88
H.
Dieng
et
al.
/
Acta
Tropica
169
(2017)
84–92
Fig.
2.
Comparison
of
mortality
rates
of
the
different
genders
of
Ae.
aegypti
when
given
equal
opportunities
to
feed
on
different
diets
for
1
week.
F,
female;
M,
male;
SUG,
sugar;
BAK,
bakery
(cake);
YOG,
yogurt;
BAN,
banana;
WAT,
water.
extracts
(MPMD
=
−41.667,
P
<
0.001),
which
showed
complete
sur-
vival
(100%).
On
day
5,
survival
responses
varied
significantly
with
diet
type
(F
=
31.65,
df
=
4,
P
<
0.001),
with
SUG
generating
the
highest
mean
rate
(100%).
This
latter
mean
survival
rate
did
not
differ
significantly
from
those
of
BAK-fed
(MPMD
=
−8.333,
P
=
0.951)
and
BAN-fed
groups
(MPMD
=
−16.667,
P
=
0.605),
which
in
turn
was
significantly
higher
than
those
of
their
peers
fed
YOG
(MPMD
=
75.000,
P
<
0.001)
and
WAT
(MPMD
=
−75.000,
P
<
0.001).
A
week
after
commencement
of
testing,
the
feeding
history
of
males
significantly
affected
their
survival
levels
(F
=
94.25,
df
=
4,
P
<
0.001).
Males
maintained
on
SUG
and
BAK
showed
similar
survival
rates
(MPMD
=
−8.333,
P
=
0.750).
These
survival
levels
obtained
from
SUG-
and
BAK-fed
males
were
appreciably
greater
than
those
of
males
under
the
YOG
(MPMD
=
−83.333,
P
<
0.001)
or
BAN
(MPMD
=
−91.667,
P
<
0.001)
regimes.
The
survival
of
YOG-
fed
females
tended
to
be
greater
than
their
counterparts
in
the
BAN
and
WAT
regimes,
but
the
difference
was
not
significant
(MPMD
=
−8.333,
P
=
0.796)
(Fig.
1A).
3.2.
Female
survival
patterns
on
different
waste-based
diets
All
Ae.
aegypti
females
fed
SUG
survived
throughout
the
obser-
vation
period.
In
the
BAK
treatment
group,
more
females
died
on
days
5
and
7
than
on
day
2,
but
the
differences
in
survival
between
days
were
not
significant
(F
=
0.50,
df
=
2,
P
=
0.611).
In
the
YOG
feeding
regime,
the
survival
rate
of
Ae.
aegypti
females
varied
with
time
(F
=
7.25,
df
=
2,
P
=
0.002).
Survival
was
100%
on
day
2,
but
decreased
markedly
thereafter,
reaching
50.00%
±
15.07%
on
day
7.
In
the
BAN
treatment
group,
survival
showed
signifi-
cant
temporal
variations
(F
=
10.82,
df
=
2,
P
<
0.001),
with
survival
rate
decreasing
sharply
from
day
2
(mean
±
SE
=
58.33%
±
14.86%)
to
day
7
(mean
±
SE
=
25.33%
±
13.05%).
When
kept
on
WAT,
Ae.
aegypti
females
exhibited
significant
variation
in
survival
rate
with
time
(F
=
28.07,
df
=
2,
P
<
0.001);
the
mean
survival
rate
was
100%
on
day
2,
75.00%
±
13.05%
on
day
5,
and
only
one
survivor
was
found
on
day
7.
For
both
SUG-fed
and
sweet
waste-fed
females,
survival
was
100%
during
the
first
two
days.
On
day
5,
SUG-
and
WAT-fed
females,
and
their
sweet
waste
extract-fed
counter-
parts
exhibited
different
survival
patterns
(F
=
2.61,
df
=
4,
P
=
0.045).
There
were
no
significant
differences
in
survival
rate
between
SUG-
fed
and
BAK-fed
(MPMD
=
−8.333,
P
=
0.979)
or
YOG-fed
females
(MPMD
=
−8.333,
P
=
0.979).
In
contrast,
BAN-fed
females
died
at
a
significantly
greater
rate
than
their
SUG-fed
counterparts
(MPMD
=
−41.667,
P
=
0.045).
The
survival
rate
of
WAT-fed
females
was
similar
to
that
of
BAN-fed
females
(MPMD
=
16.667,
P
=
0.782).
On
day
7,
the
type
of
food
supplied
to
females
significantly
influ-
enced
their
survival
(F
=
15.07,
df
=
4,
P
<
0.001).
The
SUG-
and
BAN-fed
females
showed
a
similar
survival
rate
(MPMD
=
−8.333,
P
=
0.979),
which
was
significantly
higher
than
those
of
their
coun-
terparts
maintained
on
YOG
(MPMD
=
−50.000,
P
=
0.010),
BAN
(MPMD
=
−75.000,
P
<
0.001)
and
WAT
(MPMD
=
−91.667,
P
<
0.001).
Females
fed
BAK
died
at
a
lower
rate
compared
to
YOG-fed

H.
Dieng
et
al.
/
Acta
Tropica
169
(2017)
84–92
89
Fig.
3.
Mean
(±SE)
response
times
to
a
mammalian
host
by
Ae.
aegypti
females
when
given
equal
opportunities
to
feed
on
different
diets
for
1
week.
SUG,
sugar;
BAK,
bakery
(cake);
YOG,
yogurt;
BAN,
banana;
WAT,
water.
(MPMD
=
−41.667,
P
=
0.047),
BAN-fed
(MPMD
=
−66.667,
P
<
0.001),
and
WAT-fed
females
(MPMD
=
−83.333,
P
<
0.001).
There
were
more
survivors
in
the
YOG
feeding
regime
than
on
BAN,
but
the
difference
in
survival
rate
between
these
two
groups
was
not
significant
(MPMD
=
−25.000,
P
=
0.439).
Females
kept
on
YOG
had
appreciably
higher
survival
than
their
peers
fed
WAT
(MPMD
=
−41.667,
P
=
0.047)
(Fig.
1B).
3.3.
Comparison
of
survival
patterns
between
males
and
females
on
day
7
Males
and
females
showed
similar
rates
of
survival
in
the
SUG
and
BAK
groups
(F
=
0.00,
df
=
1,
P
=
1.000).
In
contrast,
females
showed
greater
survival
than
males
when
both
were
maintained
on
YOG
(F
=
5.85,
df
=
1,
P
=
0.024).
A
similar
survival
pattern
was
also
observed
in
adults
kept
on
BAN
(F
=
3.66,
df
=
1,
P
=
0.069)
and
WAT
(F
=
1.00,
df
=
1,
P
=
0.328),
but
the
differences
between
male
and
female
survival
levels
were
not
significant
(Fig.
2).
3.4.
Patterns
of
response
time
to
host
presence
There
were
significant
variations
in
the
female
response
time
to
the
presence
of
a
host
related
to
feeding
history
(F
=
3.93,
df
=
3,
P
=
0.016).
The
mean
response
time
of
females
fed
SUG
(515.50
±
78.40
s,
range
217––890
s)
was
longer
than
any
of
those
obtained
from
sweet
waste
extract-fed
females.
The
mean
times
for
females
maintained
on
BAK,
YOG,
and
BAN
were
270.00
±
79.18
s,
217.69
±
59.19
s,
and
402.89
±
89.37
s,
respectively.
Among
these
sweet
waste
extract-fed
females,
those
fed
on
BAN
tended
to
attack
the
host
earlier
than
their
peers
maintained
on
either
BAK
or
YOG.
The
mean
response
time
for
BAN-fed
females
was
1.85
and
1.48
times
those
of
BAK-fed
and
YOG-fed
females,
respectively
(Fig.
3).
3.5.
Egg
production
in
relation
to
adult
diet
Ae.
aegypti
females
maintained
on
SUG
had
a
mean
egg
pro-
duction
rate
of
130.00
±
4.91
(range
112–143).
The
mean
numbers
of
eggs
produced
by
their
counterparts
maintained
on
BAK,
YOG,
and
BAN
were
120.00
±
7.94
(range
89–143),
110.70
±
5.49
(range
112–143),
and
121.20
±
9.23
(range
87–138),
respectively.
There
were
no
significant
differences
in
egg
production
rates
between
the
different
female
feeding
histories
[SUG
and
sweet
waste-based
extracts
(F
=
1.57,
df
=
3,
P
=
0.223)
(Fig.
4).
Fig.
4.
Mean
(±SE)
egg
production
of
Ae.
aegypti
when
given
equal
opportunities
to
feed
on
different
diets
for
1
week.
SUG,
sugar;
BAK,
bakery
(cake);
YOG,
yogurt;
BAN,
banana;
WAT,
water.
4.
Discussion
The
present
study
indicated
that
extracts
from
sweet
waste
products
can
successfully
support
adult
Ae.
aegypti
to
an
appre-
ciable
extent
relative
to
SUG,
a
classical
diet
used
in
the
laboratory
and
an
energy
source
required
daily
by
both
sexes
in
nature
(Yuval,
1992).
Feeding
on
sweet
waste
fluids
positively
affected
the
key
elements
of
vectorial
capacity
examined
in
this
study.
Of
the
diets
tested,
similar
and
increased
survival
rates
were
observed
in
males
maintained
on
SUG
and
BAK.
In
BAK-fed
females,
this
similarity
in
survival
persisted
until
day
5
after
commencement
of
testing,
and
an
appreciable
proportion
of
females
(about
25%)
were
still
alive
on
day
7.
These
observations
suggested
that
BAK
extract
fulfilled
the
energetic
requirements
of
Ae.
aegypti
adults,
especially
females.
Sugar
is
essential
for
prolonged
survival
of
both
male
and
female
mosquitoes
(Burkett
et
al.,
1998;
Joy
et
al.,
2010).
It
is
the
only
nutritional
source
for
males
and
is
a
dietary
sup-
plement
to
blood
for
females
(Ondiaka
et
al.,
2015).
In
nature,
vector
population
densities
have
been
reported
to
be
low
when
fewer
preferred
nectar
sources
are
present
and
decline
season-
ally
when
sugar
sources
decline
(Hocking,
1968;
Gadawski
and
Smith,
1992).
Without
sugar,
mosquitoes
can
die
rapidly
despite
frequent
access
to
blood
(Nayar
and
Sauerman,
1971;
Fernandes
and
Briegel,
2005).
In
aedine
species,
there
is
a
close
relationship
between
the
amount
of
sugar
and
survival
quality.
Aedes
communis
maintained
on
25%
or
50%
sucrose
or
fructose
showed
significantly
longer
survival
than
those
maintained
on
10%
sucrose
(Andersson,
1992).
Ae.
aegypti
lived
much
longer
in
the
laboratory
when
pro-
vided
with
both
sugar
and
blood
than
with
blood
alone
(Clements,
1992).
In
the
malaria
vector,
Anopheles
gambiae,
Nyasembe
et
al.
(2012)
noted
that
the
availability
of
high
levels
of
digestible
sugars
increased
survival.
Naziri
et
al.
(2016)
examined
survival
rates
of
Aedes
albopictus
females
maintained
with
sugar
at
different
con-
centrations,
and
reported
the
highest
survival
rates
with
10%
and
30%
sucrose.
In
the
present
study,
the
SUG
solution
and
the
BAK
extract
were
produced
by
soaking
5
g
of
each
substance
in
100
mL
of
water
and
by
stirring
the
brews
for
3
min.
We
exposed
Ae.
aegypti
adults
to
these
two
feeds
for
the
same
period,
which
led
to
simi-
lar
survival
responses.
Sucrose
consists
of
equal
parts
glucose
and
fructose
(Barnett
and
Garg,
2004)
and
chocolate
contains
sucrose
(Fong,
2014).
Thus,
it
is
likely
that
the
SUG
and
the
BAK
solutions

90
H.
Dieng
et
al.
/
Acta
Tropica
169
(2017)
84–92
contained
similar
levels
of
sugars,
and
the
observed
equivalence
of
survival
rates
between
the
SUG
and
BAK
feeding
regimes
was
probably
due
to
similar
levels
of
digestible
sugars.
It
is
also
possi-
ble
that
the
observed
similarities
in
survival
patterns
between
the
SUG-fed
and
BAK-fed
adults
occurred
due
to
similarities
in
uptake
frequency
and
amount.
In
mosquitoes,
deficient
uptake
of
sugar
when
it
is
available
has
been
linked
to
the
presence
of
certain
agents.
For
example,
phenolic
compounds,
such
as
flavonoids,
were
reported
to
inhibit
ecdysone
20-monooxygenase,
serine
protease,
and
trypsin
activi-
ties
in
many
insects,
including
mosquitoes
(Mitchell
et
al.,
1993).
Caffeic
acid
and
saponin
have
been
shown
to
exhibit
anti-feeding
activity
in
insect
pests
(Rani
and
Devanand,
2013).
Vanillic
and
p-
coumaric
acids
have
been
reported
to
exert
anti-feedant
activities
in
some
insects
(Pavela,
2007).
Alkaloids
act
as
feeding
deterrents
and
are
toxic
to
several
insect
species
(Wink,
1992).
Phytochemi-
cal
screening
of
banana
extracts
revealed
the
presence
of
several
compounds,
including
flavonoids,
caffeic,
vanillic,
and
p-Coumaric
acids
(Ongphimai
et
al.,
2013),
saponin
(Mahmood
et
al.,
2011),
and
alkaloids
(Ehiowemwenguan
et
al.,
2014).
Similar
to
banana,
berries
also
contain
flavonoids
and
phenolics
(Stajˇ
ci´
c
et
al.,
2012).
In
the
present
study,
the
YOG
type
used
contained
sliced
berries.
Both
the
YOG
and
BAN
extracts
were
produced
by
adding
5
g
of
YOG
concentrate
and
banana
puree
into
100
mL
of
water.
Maintenance
of
Ae.
aegypti
on
YOG
and
BAN
extracts
resulted
in
reduced
survival
rates
compared
to
SUG
and
BAK
feeding
regimes.
No
males
main-
tained
on
BAN
extract
survived
on
day
7
and
less
than
10%
were
still
alive
on
the
YOG
regime
on
the
same
day;
about
half
and
three
quarters
of
females
kept
on
YOG
and
BAN,
respectively,
died
1
week
after
commencement
of
testing.
Although
we
did
not
establish
the
chemical
profiles
of
the
tested
fluids,
the
observed
discrepancies
in
survival
responses
between
SUG
and
YOG
or
BAN
may
have
been
caused
by
differences
in
digestible
sugars
or
uptake.
Another
explanation
could
be
differential
contents
of
anti-feedant
agents.
Indeed
YOG
and
BAN
extracts
may
have
contained
greater
amounts
of
flavonoids,
caffeic,
vanillic,
and
p-coumaric
acids,
saponin,
or
alkaloids,
which
interfered
with
Ae.
aegypti
feeding.
The
feeding
deterrence
effects
of
such
compounds
seem
to
be
more
pronounced
in
BAN
extract.
Females
maintained
on
sweet
waste
extracts
exhibited
a
more
rapid
response
to
the
presence
of
a
mammalian
host
compared
to
those
kept
on
SUG.
In
particular,
females
that
were
supplied
YOG
showed
the
shortest
response
time
to
biting
the
host.
Due
to
its
direct
impact
on
virus
transfer
or
pickup
and
disease
transmis-
sion,
there
has
been
a
great
deal
of
research
regarding
host
seeking
behavior
relative
to
female
larval-inherited
nutritional
status
or
body
size
(Klowden
et
al.,
1988;
Xue
et
al.,
1995;
Nasci,
1991).
Most
of
these
studies
took
into
account
host
attack
rate,
and
did
not
examine
sugar
uptake
status
or
response
time
to
the
presence
of
a
host.
For
successful
blood
meal
uptake,
females
(including
those
of
Ae.
aegypti)
must
pre-probe
(Walker
and
Edman,
1985),
search
for
a
suitable
vessel,
and
slot
its
stylet
(Labuda
and
Kozuch,
1989;
Moreira
et
al.,
2009).
The
achievement
of
these
activities
depends
largely
on
the
defensive
reactions
of
the
host.
There
is
evidence
that
defensive
behavior
affects
mosquito
biting
rate,
thus
preventing
further
vector–host
contact
and
that
blood-feeding
success
is
neg-
atively
correlated
with
defensive
behaviors
(Walker
and
Edman,
1985;
Darbro
and
Harrington,
2007).
Biting
persistence
does
not
affect
disease
transmission
in
dengue
vectors
(Canyon
et
al.,
1998).
As
the
host
is
often
unaware
of
being
attacked
by
a
female
mosquito
on
its
first
attempt,
this
period
of
female–host
interaction
should
be
examined
as
it
is
critical
for
blood
feeding
success.
Turley
et
al.
(2009)
suggested
that
investigation
of
biting
attempts
has
the
potential
to
provide
information
regarding
an
insect’s
capacity
to
vector
pathogens.
Clearly,
first
attacks
from
females
will
tend
to
result
in
a
greater
chance
of
overcoming
defensive
reactions
and
thus
blood
uptake
success;
later
attacking
females
are
more
likely
to
experience
unsuccessful
landing,
disturbance,
shaking,
and
dis-
lodging
from
the
host.
These
reactions
may
lead
to
unsuccessful
blood
feeding.
Therefore,
we
examined
response
time
to
host
pres-
ence
taking
into
account
female
diet.
Our
observations
indicate
that
BAK-,
YOG-,
and
BAN-fed
females
initiated
host
attack
much
ear-
lier
than
females
from
the
SUG
treatment
group.
These
findings
corroborate
the
earlier
reports
indicating
the
importance
of
sugar
level
in
regulating
the
initiation
time
of
host
seeking
and
attack.
Starved
female
Ae.
albopictus
mosquitoes
showed
a
shorter
time
to
host
attack
compared
to
those
fed
sugar
(Dieng
et
al.,
2015).
In
another
study,
Klowden
(1986)
noted
an
increase
in
host
attack
behavior
of
carbohydrate-deprived
Ae.
aegypti
females
in
contrast
to
those
maintained
on
sucrose.
Taken
together,
these
reports
sug-
gest
that
hunger
level
plays
a
key
role
in
response
time
to
the
host.
In
the
present
study,
Ae.
aegypti
mosquitoes
were
fed
four
different
diets,
i.e.,
SUG,
BAK
(chocolate
cake),
YOG,
and
BAN.
Overall,
two
patterns
of
response
time
to
host
were
obtained:
SUG-maintained
females
took
a
long
time
to
initiate
host
biting,
while
those
main-
tained
on
sweet
waste
extracts
(BAK,
YOG,
and
BAN)
showed
a
significantly
shorter
response
time,
which
did
not
differ
between
them.
Cocoa,
the
main
ingredient
of
chocolate,
contains
flavonoids
(Miller
et
al.,
2008)
and
alkaloids,
such
as
caffeine
(New
South
Wales
Government,
2015),
which
are
known
to
inhibit
feeding
behaviors
in
some
insects
(Araque
et
al.,
2007).
Such
chemicals
are
also
present
in
banana
(Ongphimai
et
al.,
2013;
Ehiowemwenguan
et
al.,
2014)
and
berries
(Stajˇ
ci´
c
et
al.,
2012),
but
not
in
sucrose.
It
is
likely
that
the
three
sweet
waste
extracts
contained
these
chemicals,
and
it
is
therefore
likely
that
females
maintained
on
BAK,
YOG,
and
BAN
regimes
have
been
in
contact
with
such
anti-
feedants.
Thus,
the
short
response
time
to
the
presence
of
a
host
in
the
sweet
waste
extract-fed
females
may
have
been
due
to
low
energy
levels
as
a
result
of
low
sugar
uptake
caused
by
the
anti-
feeding
effects
of
such
compounds.
The
observed
short
response
time
of
females
fed
BAK,
YOG,
and
BAN
is
a
possible
indicator
of
hunger
and
a
strategy
to
compensate
for
their
deficient
energy
lev-
els.
Ae.
aegypti
females
are
active
during
the
day
(Harrington
et
al.,
2008),
when
human
hosts
are
also
active.
Theoretically,
the
rapid
response
to
the
host
observed
in
BAK-,
YOG-,
and
BAN-fed
females
is
likely
to
be
associated
with
increased
blood
meal
uptake
chances,
which
will
tend
to
increase
the
likelihood
of
disease
occurrence.
In
support
of
this
suggestion,
sugar-unfed
or
sugar-deficient
females
of
Anopheles
(Straif
and
Beier,
2008;
Gary
and
Foster,
2001)
and
Ae.
aegypti
(Jahangir
et
al.,
2008)
were
reported
to
exhibit
increased
blood
feeding
activities.
Despite
differences
in
timing
of
responsiveness
to
the
host,
both
SUG-fed
and
sweet
waste-supplied
females
showed
similar
fecun-
dity.
It
is
generally
believed
that
females
use
some
proteins
(Hill,
2013)
and
iron
(Zhou
et
al.,
2007)
found
in
blood
meals
to
make
their
eggs.
The
role
of
sugar
diet
in
mosquito
egg
production
has
been
well
documented.
Overall,
sugar
has
a
strong
influence
on
ovarian
development
(O’Meara,
1985;
Abraham,
2013),
rate
of
egg
development
(Andersson,
1992),
and
egg
clutch
size
(Nayar
and
Sauerman,
1975).
In
the
species
studied
here,
Mostowy
and
Foster
(2004)
assessed
egg
production
in
females
under
conditions
of
dif-
ferent
sugar
intake
status.
The
number
of
eggs
produced
decreased
from
blood-fed
females
with
full
crops
and
low
energy
reserves,
to
females
with
full
crops
and
high
energy
reserves,
to
those
with
empty
crops
and
high
energy
reserves.
Briegel
(1985)
reported
that
fecundity
is
positively
correlated
with
the
amount
of
blood
ingested,
which
in
turn
is
closely
associated
with
sugar
feeding
sta-
tus.
Thus,
the
equivalent
egg
production
observed
in
SUG-fed
and
sweet
waste
fluid-fed
females
suggested
that
they
may
have
taken
equivalent
amounts
of
blood
meals.

H.
Dieng
et
al.
/
Acta
Tropica
169
(2017)
84–92
91
5.
Conclusions
This
study
was
performed
to
examine
the
perceptual
nutri-
tional
significance
of
sweet
waste
fluids
on
Ae.
aegypti
with
respect
to
prospective
epidemiological
implications.
Our
investi-
gation
revealed
the
capacity
of
sweet
waste-derived
extracts
(at
least
BAK)
to
sustain
Ae.
aegypti
of
both
sexes
in
a
manner
simi-
lar
to
that
of
sugar,
the
classical
mosquito
diet.
Furthermore,
the
results
presented
here
indicated
that
maintenance
on
sweet
waste
extracts
resulted
in
increased
responsiveness
to
the
presence
of
a
host
compared
to
sugar
uptake.
Eventually,
SUG-fed
and
sweet
waste-fed
females
showed
comparable
levels
of
egg
production.
These
effects
indicated
the
potential
of
sweet
leftover
food-derived
fluids
to
positively
influence
the
energy
reserves
and
thus
some
key
traits
of
the
vectorial
capacity
of
a
dengue
vector.
Huge
amounts
of
food
waste
are
produced
every
day
(Gustavsson
et
al.,
2011;
Nation,
2016).
According
to
the
UN
Food
and
Agricultural
Orga-
nization,
between
one
third
and
one
half
of
all
food
produced
goes
uneaten.
Many
different
sweet
items,
such
as
fruits,
cakes,
desserts,
and
dairy
and
bakery
products,
have
been
identified
in
garbage
sites
(WRAP,
2009).
Food
waste
is
a
growing
problem
in
the
urban
cen-
ters
of
many
countries
in
Asia
(da
Silva,
2016),
and
the
same
is
also
true
of
dengue
(Ooi
and
Gubler
2009;
Akhtar,
2016).
When
partly
eaten
fruits,
such
as
bananas
with
the
skin,
yogurt
cups,
or
plastic
cake
containers
with
remnants,
are
discarded
outdoors
and
are
uncollected
from
garbage
sites,
they
can
collect
rainwater
and
generate
sweet
solutions
such
as
those
studied
here,
on
which
mosquito
adults
can
feed.
Most
Asian
countries
have
a
long
history
of
waste
management
problems,
and
despite
education
and
policy
making
efforts
the
amount
of
waste,
including
unfinished
foods,
has
not
decreased
due
to
excessive
purchasing,
improper
attitudes
with
regard
to
discarding
of
waste,
and
insufficient
disposal
facil-
ities.
Our
study
was
prompted
by
the
discovery
of
a
partly
eaten
apple
and
Kit
Kat
chocolate
bar
holding
water
in
some
garbage
sites
in
Malaysia.
This
observation,
combined
with
our
results
showing
positive
impacts
of
sweet
waste
fluids
on
both
sexes
of
Ae.
aegypti
suggest
that
such
types
of
refuse
contribute
to
the
persistence
of
wild
dengue
vector
populations
across
Southeast
Asia
and
similar
regions.
This
is
presumably
the
case
for
Anopheles
and
Culex
vec-
tors,
which
also
use
sugar
as
staple.
Reducing
the
prevalence
of
such
sweet
waste
items
in
nature
is
relevant
to
any
vector
con-
trol
strategy
targeting
these
mosquito
vectors,
as
these
items
can
act
as
man-made
nectar
sources.
Anti-mosquito
awareness
educa-
tion
activities
emphasizing
the
importance
of
proper
waste
disposal
behaviors
and
knowledge
regarding
the
nutritional
ecology
of
adult
mosquitoes
are
required.
Acknowledgments
The
authors
are
grateful
to
Ms.
Bailey
Munro
(Canada)
and
Rani
Karyani
(Indonesia)
for
their
assistance
in
mosquito
colony
estab-
lishment
and
maintenance.
This
work
was
supported
by
a
grant
from
The
Department
of
Microbiology,
Faculty
of
Pharmaceutical
Sciences,
Fukuoka
University,
Japan.
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