Natural History, Ecology and Evolution of Aedes aegypti and Aedes

Natural History, Ecology and Evolution
of Aedes aegypti and Aedes albopictus
with Special Reference to Florida
P Lounibos, Univ. of Florida,
Florida Medical Entomology Lab
Part I: Invasion Biology &
Competitive Displacement
Part II: Natural History &
Ecology of Life Stages in Florida
Part III: A Resurgence of
A. aegypti in Florida?
Major range expansion of Aedes albopictus
occurred in the past 40 years from Asia
1991
1985
1991
1985
Enserink. 2008. Science
These two species both frequent container habitats provided by
humans and, as adults, mate in association with host-seeking
Rapid disappearance
of A. aegypti in Bermuda
after establishment of
A. albopictus
Ex Kaplan et al. (2010) Biological Invasions
Decline of A. aegypti after the arrival of A. albopictus in
Florida
Lake city
Gainesville
Ocala
Leesburg
Apopka
Orlando
Kissimmee
St. Cloud
Yeehaw Junction
Okeechobee
Modified from O’Meara et al. J. Med. Entomol. 1995
Surveillance in south Florida cemeteries since 1990 documented
rapid displacement and led to testing hypotheses
of proposed mechanisms
Patterns of exclusion and co-existence in south Florida
cemeteries (modified ex Lounibos et al. 2010 An. Entomol. Soc. Am.)
Larval densities, leaf litter, and species were manipulated in experiments
in tires and plastic cups in Vero Beach, Florida and Rio de Janeiro, Brazil
2004
(Braks et al. 2004)
Auto salvage yards harbor sympatric A. albopictus and A. aegypti
in south Florida
Evidence of interspecific mating
among field-collected females
Sperm from
Collection
Site
M& K Auto
Species
aegypti
Mean No.
(SE) Per Coll
73.4 (18.7)
(n=7)
albopictus
Belle Glade
(n=2)
Spermathecae
Totals
85
A.
albopictus
0
161.0(60.0)
1
71
72
aegypti
67.5(2.5)
82
3
85
albopictus
411.5(170.5)
1
61
62
169
135
304
Totals
A.aegypti
85
Ex: Tripet et al. (2011) Am. J. Trop. Med. Hyg.
Sperm extracted from field-collected females
and DNA amplified
Hypothesis: Male accessory gland (MAG) products
of A. albopictus asymmetrically sterilize A. aegypti
Science 156: 1499-1501 (1967)
Experiment:
1. Inject MAG homogenates from conspecific or
heterospecific males into unmated females of both
species.
2. Allow post-injection females access to conspecific
males in cages.
3. Assess insemination rates by spermathecal
dissections
Results (Tripet et al. [2011] AJTMH 85) confirmed that the sterilizing effects
of MAG extracts are asymmetric in their interspecific effects
Reproductive Character Displacement
= phenotypic evolution in a population caused by
cross-species mating and which results in enhanced
prezygotic reproductive isolation between sympatric
species.
(Grether et al. 2009, Biol. Rev. 84)
Hypothesis: Aedes aegypti which remain in
sympatry with A. albopictus will evolve a
mechanism(s) to avoid wasteful interspecific
matings
Experiment: compare frequencies of
interspecific matings in cages of allopatric
vs. sympatric populations of the two species
from the USA
Cage Trials of Interspecifc Matings between Populations
100
Mean (± SE) percentage of females
inseminated
90
80
70
60
50
Females: A. aegypti
Allopatric females
source
χ2(1)
female origin 25.3***
male origin
0.1ns
female X male 0.1ns
block(2)
30.9***
Sympatric females
Females: A. albopictus
Allopatric females
source
χ2(1)
female origin 47.7***
male origin
3.0ns
female X male 4.4*
block(2)
1.3ns
Sympatric females
40
30
20
10
0
Allopatric Sympatric Allopatric Sympatric Allopatric Sympatric Allopatric Sympatric
Males: A. albopictus
Males: A. aegypti
Ex Bargielowski et. al. (2013) PNAS
Percentage (± s.e.) of females
inseminated
70
60
Allopatric populations of
50
40
30
KW
A. aegypti females exposed
KW
control
to A. albopictus males evolve
20
10
0
resistance to interspecific
mating in a few generations
70
60
50
40
Miami
30
20
Miami
control
10
0
Bargielowski & Lounibos (2013) Evol Ecol
Factors contributing to competitive displacement and
segregation of Aedes aegypti by Aedes albopictus
U
N
F
A
V
O
R
A
B
L
E
LARVAL
COMPETITION
rural
SATYRIZ ATION
+
albopictus
(invader)
C
L
I
M
A
T
E
HABITAT
SEGREGATION
aegypti
albopictus
& aegypti
(resident)
suburban
-
 30° Ν
urban
1985
ARRIVAL &
ESTABLISHMENT
L
A
T
I
T
U
D
E
 25° Ν
Natural History &
Ecology of Life Stages in Florida
• Eggs:
A. albopictus
A. aeg ypti
Desiccation-resistance of aedine
eggs influences what habitats may be
colonized. All species shown
(3 included as ‘forest’) belong to the
subgenus Stegomyia. Numbers refer
to different geographic strains. (ex:
Sota & Mogi 1992. Oecologia 90:353-358)
Aedes eggs, laid on tongue depressors
Depressors with eggs
of each species in a
screened vase
1.0
2001
A. aegypti
A. albopictus
% Hatch (SE)
0.8
0.6
2006
***
***
0.4
***
**
0.2
0.0
2 weeks.
4 weeks.
2 weeks
4 weeks
Weeks of Exposure
Lounibos et al. 2010 An. Entomol. Soc. Am.
MANOVA for 2001 Microclimate PCs:
Effect
DF
Pillai’s Trace
F
P
Cemetery 15,54
2.046
7.72
<0.001
Type
0.923
64.16
<0.001
Factor 2
High
rhmax, rhmean
3,16
4
2
0
A. aegypti
persists
-2
-4
-4 Low
rhmin
-2
0
Factor 1
2
High 4
tmax, tmean
Lounibos et al. 2010 An. Entomol. Soc. Am.
14L : 10D
21oC
Assay eggs for diapause
10L : 14D
Photoperiodic egg diapause occurs in all Florida
populations of A. albopictus tested
Site
Lat.(°N)
E. St. Louis 38° 38´
Pensacola 30° 25´
Cottondale 30° 48´
Jacksonville 30° 19´
Vero Beach 27°35´
Miami
25°45´
Card Sound 25°25´
% Hatch (no. eggs) 1998-20001
14L:10D
10L:14D
92.3 (1,359)
0.6 (1,511)
98.2 (979)
89.4 (1,390)
91.3 (403)
91.0 (600)
99.4 (325)
1.2 (1,241)
8.9 (1,267)
13.1 (381)
30.3 (892)
23.3 (365)
% Hatch (+SE) 2008
14L:10D
10L:14D
91.0 (4.9) 6.9 (2.6)
98.6 (0.5) 3.2 (0.6)
97.7 (0.8)
83.6 (14.5)
95.5 (0.8)
96.5 (1.4)
6.6 (1.9)
66.1(3.3)
69.4(3.9)
20.7(4.5)
Ex Lounibos et al. 2011 JAMCA 27: 433-436
Short-day (diapause) eggs survive south Florida
winter better than long-day (non-diapause) eggs
Ex Lounibos et al. 2011 JAMCA 27: 433-436
Quiescence and Diapause in Aedine Eggs
• Quiescence = inactivity owing to unfavorable
environment
- flooding, especially with deoxygenated water,
stimulates hatch
- conditioning influences hatchability
Diapause eggs will not hatch with flooding alone,
and require reactivation (=diapause termination)
- obligate state in univoltine species
- facultative in temperate, multivoltine species
% Hatch
No. Hatch Stimulus
Among treehole mosquitoes on the Kenya Coast, most eggs of Aedes aegypti
hatched after first flooding
(Ex. Lounibos 1981. Ecol. Entomol.6)
Habitat Segregation in South Florida Ovitraps
number of mosq.
2000
A. aegypti
1500
WPB
BR
1000
500
!
0
urban
suburban
rural
number of mosq.
2000
A. albopictus
1500
WPB
BR
1000
500
!
0
urban
suburban
rural
Ex Braks et al. 2003 J. Med Entomol
40: 785-794.
Ovitrap abundances of the two species in three south Florida counties
were associated in opposite directions to compound habitat variables
quantified from aerial images
Ex Rey et al. (2006) J. Med Entomol. 43:1134-1141
Florida Keys
2002-09
Aedes aegypti
Ex Hribar
& Whiteside
(2010)
Both species
occur throughout
the year in south
Florida
FMEL Treeholes
1991-2003
Ex Lounibos
& Escher (2008)
Natural History &
Ecology of Life Stages in Florida
Aquatic Stages:
Container Habitats Producing A. aegypti Pupae in the Florida Keys
Ex Hribar & Whiteside (2010)
Stud Dipteralog 17:237-251
Ex Lounibos et al. (2003) Ecol. Entomol. 28
0.8
% Survival A. albopictus
0.7
F-stats
Litter
Wyeomyia
Litter x Wyeomyia
6.68*
25.95***
4.57(ns)
0.6
0.5
0.4
0.3
0.2
0.1
S2
0
+
1
Wyeomyia
S1
-
2
-
Litter
+
Ecological homologs
co-occurring in eastern USA
Aedes albopictus
(invasive)
Aedes triseriatus
(native)
Dipterous predators in Florida treeholes preferentially
consume A. albopictus over A. triseriatus
T. rutilus IV consuming
Aedes sp. IV instar
C. appendiculata IV
consuming Aedes sp. II
How is predation success of C. appendiculata
influenced by prey (A. albopictus) behavior?
Significant differences (P<0.0001) in activities (χ2(3)=25.04)
and positions (χ2(3)= 45.73)
Kesavaraju et al. 2007 Ecological Entomology
Thrashing, Bottom
Browsing,
Resting, Surface
The behavior of native treehole larvae, but not the invasive, changes
in the presence of water-borne cues of C. appendiculata IV
1.5
1.0
b
Control
Predation
0.5
0.0
a
-0.5
-1.0
a
Aedes albopictus
a
Aedes triseriatus
-1.5
Kesavaraju et al. 2007 Ecological Entomology
Prediction – multigeneration
field experiment –
(open to immigration):
C. appendiculata will reduce
the invasability of naturally
exposed tires by A. albopictus
and facilitate coexistence
with A. triseriatus
Containers & Setting: Golf cart tires with sieved
tire water and 2.0 g oak leaves, arranged in
groups of four at eight random sites in hammock
Treatments (4):
- control (no added macroinvertebrates)
- 100 I A. triseriatus
- 100 I A. triseriatus + 2 IV C. appendiculata
- 100 I A. triseriatus + 8 IV C. appendiculata
Census every nine days, adding supplementary A.
triseriatus Is and C. appendiculata IVs
Repeat in summers of 2005 & 2006
Mean A. albopictus per tire ( SE)
50
2006
Control
Competitor
Low Predator (2)
High Predator (8)
40
30
20
10
0
9
18
27
Days of observation
Both low and moderate-density predator treatments suppressed
colonization of tires by A. albopictus (Juliano et al. 2010 Oecologia)
50
2005
2006
Aedes albopictus eggs
40
30
20
10
0
CONTROL
COMPETITOR
LOW PRED.
HIGH PRED.
Treatment
Juliano et al. 2010 Oecologia 162
Natural History &
Ecology of Life Stages in Florida
Adults:
What are the bloodmeal hosts of these species in nature?
Blood Meal Analyses of Wild-caught Aedes
aegypti
Location
Dominant Host
Reference
Kenya
Reptiles
McClelland & Weitz 1963
Thailand
Humans
Ponlawat & Harrington 2005
USA (Hawaii) Humans
Tempelis et al. 1970
USA (PR)
Scott et al. 2000
Uganda
Humans
Rodents
McClelland & Weitz 1963
Blood Meal Analyses of Wild-caught Aedes
albopictus
Location
Brazil
Dominant Host
Humans, cows
Spain
Humans
Muňnoz et al. 2011
Thailand
Humans
Ponlawat & Harrington 2005
USA (Hawaii) Humans
Reference
Gomes et al. 2003
Tempelis et al. 1970
USA (Illinois) Rabbits & Rats
USA (Missouri) Rabbits
Niebylski et al. 1994
Savage et al. 1993
Is Superior Reproductive Success on Human
Blood without Sugar Limited to Aedes aegypti?
No! Both Species May Utilize This Strategy (Braks et al. 2006)
Evidence for Multiple Blood Meals
per Gonotrophic Cycle Based on
Dissections of Biting Females
% of A. albopictus
with eggs:
Thailand 19% (n=2341)
Singapore 8% (n=631)
Kenya data from Trpis &
Hausermann 1986
Thai data from
Gould et al. (1970);
Singapore from
Chan (1971)
Activity Rhythms of Female Aedes aegypti:
Jones, 1981, Physiol. Entomol. 6
Dispersal of gravid A. aegypti, marked with Rb, in Rio de Janeiro
Ex Honorio et al. 2003 Mem. Inst. Osw. Cruz 98
Dispersal of gravid A. albopictus, marked with Rb, in Rio de Janeiro
Ex Honorio et al. 2003 Mem. Inst. Osw. Cruz 98
Installment oviposition of A. aegypti from Puerto Rico
a.) Means of Individual females
b.) means of ten females
Ex Reiter 2007 VBZD
In experiments in outdoor cages, Rey & O’Connell (2014) found
both skip oviposition and laying eggs on the water surface to be
more common in A. aegypti than A. albopictus
Will Satyr-resistant Aedes aegypti Recover in Florida?
AFTER ~20 YR OF ABSENCE, A. AEGYPTI RECENTLY DETECTED
IN THREE SUBURBAN-RURAL SOUTH FLORIDA CEMETERIES
SSix parallel collecting transects established from
the coast to inland in Palm Beach County, Florida
Kriged
distribution of
Ae. aegypti
0%
transparency
Color intensity
internally
consistent
within
sampling
period
Reiskind & Lounibos 2012
Med. Vet. Entomol.
Five Year Comparison
Interpolated landscape in 2006 & 2007
(proportion A. aegypti; brown = A.
albopictus, blue = A. aegypti)
Interpolated landscape in 2013
(proportion A. aegypti; brown = A.
albopictus, blue = A. aegypti)
100
NS
NS
% Aedes aegypti (n=6 sites)
90
NS
Mean % A. aegypti in 2013
80
p<0.009
70
Mean % A. aegypti in 2006 & 2007
60
50
40
30
20
NS
10
0
0
1
2
3
4
5
6 7 8 9 10 11 12 13 14 15
Kilometer from Coast
Paired T-tests on proportion A. aegypti (df=5)
Courtesy M. Reiskind NCSU
Selected References
Christophers SR. 1960. Aedes aegypti (L.) The Yellow Fever Mosquito. Its Life History,
Bionomics and Structure. Cambridge University Press, UK.
Hawley WA. 1988. The biology of Aedes albopictus. Journal of the
American Mosquito Control Association 4 (Supplement #1): 1-39.
Silver, JB. 2008. Mosquito Ecology. (3rd edition). Springer, NY