Life cycle and reproductive patterns of Triatoma ru brovaria
( Blanchard, 1 8 4 3 ) ( Hemiptera: Reduviidae) under constant and
fluctuating conditions of temperature and humidity
Ciclo de vida e características reprodutivas de
Tria to m a rubro va ria
( Blanchard, 1 8 4 3 ) ( Hemiptera: Reduviidae) em condições constantes
e variáveis de temperatura e umidade
Miryam P. Damborsky
1, María E. Bar
1and David Gorla
2ABSTRACT
The a im o f this study wa s to e va lua te the te m pe ra ture a nd re la tive hum idity influe nce in the life cycle , m o rta lity a nd fe cundity pa tte rns o f Triatoma rubrovaria. Fo ur co ho rts with 60 re ce ntly la id e ggs e a ch we re co nfo rm e d. The co ho rts we re divide d into two gro ups. In the co ntro lle d co nditio ns gro up inse cts we re m a inta ine d in a da rk clim a tic cha m b e r unde r co nsta nt te m pe ra ture a nd hum idity, whe re a s tria to m ine s o f the a m b ie nta l te m pe ra ture gro up we re m a inta ine d a t ro o m te m pe ra ture . Ave ra ge incub a tio n tim e wa s 15.6 da ys in the co ntro lle d co nditio ns gro up a nd 19.1 da ys in the a m b ie nta l te m pe ra ture . In gro up co ntro lle d co nditio ns the tim e fro m e gg to a dult de ve lo pm e nt la ste d 10 m o nths while gro up a m b ie nta l te m pe ra ture to o k fo ur m o nths lo nge r. Egg e clo sio n ra te wa s 99.1% a nd 98.3% in co ntro lle d co nditio ns a nd a m b ie nta l te m pe ra ture , re spe ctive ly. To ta l nym pha l m o rta lity in co ntro lle d co nditio ns wa s 52.6% whe re a s in a m b ie nta l te m pe ra ture wa s 51.8%. Me a n num b e r o f e ggs/ fe m a le wa s 817.6 co ntro lle d co nditio ns a nd 837.1 a m b ie nta l te m pe ra ture . Fluctua ting te m pe ra ture a nd hum idity pro m o te d cha nge s in the life cycle dura tio n a nd in the re pro ductive pe rfo rm a nce o f this spe cie s, a ltho ugh no t in the spe cie s m o rta lity. Ke y-words. Li f e c yc le . Re p ro d u c ti ve c h a ra c te ri sti c s. Te m p e ra tu re . Hu m i d i ty. Tr iato ma r ub r o var ia.
RESUMO
O presente tra ba lho teve co m o o bjetivo a va lia r a influência da tem pera tura e um ida de rela tiva so bre o ciclo bio ló gico , m o rta lida de e fecundida de de Triatoma rubrovaria. Fo rm a ra m -se qua tro co o rtes, ca da um a de 60 o vo s recentem ente co lo ca do s. As co o rtes fo ra m dividida s em do is grupo s: O grupo co ndiçõ es co ntro la da fo i m a ntido em estufa co m tem pera tura e um ida de co nsta ntes, e o grupo tem pera tura a m bienta l fo i m a ntido em co ndiçõ es va riá veis de tem pera tura e um ida de. O tem po de incuba çã o do s o vo s fo i de 15.6 co ndiçõ es co ntro la da e de 19.1 dia s tem pera tura a m bienta l. O perío do de desenvo lvim ento de o vo a a dulto fo i de dez m eses em co ndiçõ es co ntro la da e 4 m eses m a is extenso em tem pera tura a m bienta l. A ta xa de eclo sã o fo i 99.1% em co ndiçõ es co ntro la da e 98.3% em tem pera tura a m bienta l. A fecundida de fo i 817.6 co ndiçõ es co ntro la da e 837.1 tem pera tura a m bienta l. O percentua l de m o rta lida de ninfa l fo i 52.6% no grupo co ndiçõ es co ntro la da e 51.8% no grupo tem pera tura a m bienta l. As va ria çõ es de tem pera tura e um ida de rela tiva exercem influência no ciclo bio ló gico e em a lguns pa drõ es repro dutivo s desta espé cie, m a s nã o em sua m o rta lida de. Pal avr as-chave s: Ci c lo b i o ló gi c o . Pa d rõ e s re p ro d u ti vo s. Te m p e ra tu ra . Um i d a d e . Tr iato ma r ub r o var ia.
1 . Depar tamento de B io lo gía, Fac ultad de Cienc ias Exac tas y Natur ales y Agr imensur a, Univer sidad Nac io nal del No r deste, Co r r ientes, Ar gentina. 2 . CRILAR – CONICET, Anillac o , La Rio j a, Ar ge ntina.
Addr e ss to: Lic . Mir yam P. Damb o r sk y. Cáte dr a de Ar tr ó po do s, Fac ultad de Cie nc ias Exac tas y Natur ale s y Agr ime nsur a. Unive r sidad Nac io nal de l No r de ste . Av da Lib e r tad 5 4 7 0 , ( 3 4 0 0 ) Co r r ie nte s, Ar ge ntina.
Fax: 5 4 3 7 8 3 4 7 - 3 9 3 0 .
e -mail: mdamb o r @ e xa. unne . e du. ar Re c e b ido e m 1 6 /1 1 /2 0 0 4 Ac e ito e m 6 /6 /2 0 0 5
Tr i a to m a r u b r o va r i a ( B l a n c h a r d, 1 8 4 3 ) i s wi de l y distributed in the Argentina Mesopotamia, Uruguay and South of Brazil8. Its presenc e in the provinc e of Corrientes ( Argentina)
was verified in basaltic outc rops of the Merc edes department4.
In Brazil it has been oc c asionally enc ountered in domestic and
peridomestic environments in rural areas of the Paraná and Río Grande do Sul States, inc reasing its presenc e in human dwellings
is a generalist spec ies feeding fro m a wide variety o f ho sts
inc luding humans, and its c o mpe te nc e as Tryp a n o so m a c ru zi
ve c to r has b e e n e xpe r ime ntally ve r ifie d2 2 0 2 3.
Higher temperature and lower relative humidity are c limatic
fac tors that dec rease the development time from egg to adult of
Chagas disease vec tors7, promoting a higher population density,
an inc rease in the feeding frequenc y and an expansion of the geographic distribution9 1 0 2 1.
The influenc e of temperature on the biology of Tria to m a rub ro va ria as well as in other Triatominae spec ies has been r e po r te d6 1 1 1 3 1 8 1 9 2 2. Studie s o n c o ld r e sistanc e sho we d that
T. ru b ro va ri a was the mo st affe c te d amo ng a numb e r o f Tr iato m inae spe c ie s5. Ho we ve r, the r e is little info r m atio n
c onc erning the development of Chagas disease vec tors under
fluc tuating temperature and relative humidity1 5.
The aim of the present study was to evaluate the temperature
and relative humidity influenc e on the life c yc le and mortality and reproduc tive patterns of T. rub ro va ria.
MATERIAL AND METHODS
A total of 93 T. rubrovaria ( 6 N1; 15 N2; 17 N3; 25 N4 and 30 N5) were c aptured in an area of natural roc k piles, loc ated 3 7 km
from Merc edes City ( 2 9 º 2 3 ' S, 5 7 º 5 0 ' W) in the provinc e of
Corrientes, Argentina. The investigation was c arried out with the
first generation offspring from Oc tober 2 0 0 0 to August 2 0 0 3 .
Four c ohorts with 6 0 rec ently laid eggs ( 0 -4 8 hours old)
eac h were c onformed. The eggs were kept in 6 0 c m3 plastic
c ontainers until all those that were viable hatc hed. The c ohorts
were divided into two groups: c ontroled c onditions ( CC) and ambiental temperature ( TA) . The nymphs were transferred into
3 0 0 c m3 glass c ontainers. The jars were c overed with nylon mesh
and provided with vertic ally plac ed strips of Whatman paper
n° 4 to allo w inse c ts ac c e ss to the fo o d r e so ur c e and fo r
absorption of exc ess humidity. The spec imens of both groups
were fed weekly on c hic kens during 3 0 minutes.
The CC gr o up inse c ts we r e maintaine d in a dar k c limatic
c ha m b e r unde r c o ns ta nt te m pe r a tur e a nd hum idity. The
tr iato mine s o f the TA gr o up we r e maintaine d unde r r o o m
te mpe r atur e and humidity with a pho to pe r io d o f 1 2 L:1 2 D hr.
Th e te m p e r a tu r e a n d h u m i d i ty we r e m e a s u r e d wi th a
We athe r link -Mo nito r II – Davis we athe r statio n.
Adult c o uple s we r e plac e d in individual c o ntaine r s to
e va lua te fe c undity. Egg ha tc hing wa s r e c o r de d da ily a nd
e c dysis, mo r tality, fe c undity and fe r tility we r e no te d we e k ly.
The rate of total nymphal mortality ( TNM) was c alc ulated as
the ratio between the number of dead nymphs of all stadia ( d
t)
and the number of living nymphs at time t ( N
t) , and it was
expressed as a perc entage using the formula: TNM= d
t /Nt x 1 0 0 .
The ab so lute nymphal mo r tality ( ANM) was e stimate d as
the r atio b e twe e n the numb e r o f de ad nymphs o f a spe c ific
nymphal stage ( d
x) and the to tal numb e r o f nymphs o f that
stage ( N
x) x 1 0 0 : ANM= dx /Nx x 1 0 0 .
Lo nge vity was me asur e d as the time e lapse d sinc e e ac h
individual mo ulte d to the adult stage until its de ath.
The fec undity was obtained as the ratio between all laid eggs and the total number of females. The fertility was c alc ulated as
the number of hatc hed eggs of the total number of laid eggs.
Statistical analysis. Analysis of variance ( ANOVA) was used to compare developmental time, mortality, longevity, number of eggs/
female/week and number of reproductive weeks between groups. The variables were transformed to log ( x+ 1 ) or hyperbolic arcsine.
Post-hoc comparisons were made using the Duncan test. Male-female
ratio was compared using chi-square test. Fecundity, fertility and
first oviposition age between groups were statistically measured by the Kruskall-Wallis test. The test for difference of proportions was
used to compare the egg survival between groups. Pearson coefficient
( r) was used to analyze the correlation between monthly fecundity
of the TA couples and monthly mean temperature. All data obtained were analyzed at a 5% significance level. Statistical analysis was carried
out with the program INFOSTAT 2 0 0 2 , version 1 .112.
RESULTS
The temper atur e in the c limatic c hamber was 2 8 ° ± 2 .2 ° C
( me an ± standar d de viatio n) , me an r e lative humidity was
6 3 % ± 6 .2 % . The mean ro o m temperature was 2 6 .1 ° ± 2 .8 ° C.
Ove r 3 ye ar s, the te mpe r atur e fluc tuate d b e twe e n 2 0 .6 ° C and 3 0 .8 ° C, the ab so lute minimum was 1 6 .9 ° C and the maximum
3 3 .1 ° C ( Figure 1 ) . Mean relative humidity was 5 5 .8 % ± 5 .6 % ,
var iatio ns r ange d fr o m 4 4 .3 % to 7 0 % , the ab so lute minimum was 3 0 % and the maximum 7 9 % ( Figur e 2 ) .
Tria to m a rub ro va ria of the TA group c ompleted one egg to adult c yc le from Oc tober 2 0 0 0 to Dec ember 2 0 0 1 . During this
period, the mean room temperature fluc tuated between 2 2 .1 °
and 2 8 .2 ° C. In nine of these 1 5 months, the temperature was
less than 2 6 ° C and the relative humidity lower than 5 6 % . The lowest absolute temperature values ( 2 2 .1 ° C and 2 3 .6 ° C) were
rec orded from May to September 2 0 0 1 .
De ve lo pme nt time . The ave r age inc ub atio n time was 1 5 .6 days in CC gr o up and 1 9 .1 days in TA ( Tab le 1 ) . Se ve nty-five pe r c e nt o f the e ggs hatc he d b e twe e n 1 5 and 1 6 days in
the CC, while tho se in gr o up TA to o k b e twe e n 1 8 and 2 1 days.
20 22 24 26 28 30 32
Jan Feb Mar Ab May Jun Jul Ag Set Oct Nov Dec
Months
T
e
mp
er
at
u
re
(°
C
)
2000 2001
2002
2003
The mean development time of eac h nymphal stage was significantly different within the groups ( F
5 , 1 2= 3 9 0 .3 0 , p< 0 .0 0 0 1 ) ,
as well as between groups ( F
1 , 1 2= 8 9 .8 8 , p< 0 .0 0 0 1 ) . The highest
variation was observed in the third ( N3 ) , fourth ( N4 ) and fifth nymphal development ( N5 ) ( p< 0 .0 5 ) . In group TA the fifth
nymphal instars took 6 9 days longer than the CC group to reach
the adult stage. In group CC the time from egg to adult development
lasted 1 0 months while group TA took four months longer.
Nymphal rec ruitment differed by one week between groups
until the thir d nym phal stage . Fr o m the fo ur th stage the rec ruitment rate was lower in group TA. Fifth stage rec ruitment
took 1 6 weeks in CC group while group TA took 3 9 weeks.
In CC the fifth nymphal instars took 4 1 weeks to reac h the
adult stage, whereas in TA they moulted to adults in just 1 0 weeks.
The male to female ratio was 1 :1 .5 in CC and 1 :1 .2 in TA, no
signific ant differenc e was observed (
χ
2 = 0 .0 4 , p= 0 .8 4 0 4 ) .Sur viva l– Mo r ta lity. The e gg e c lo sio n r ate was 9 9 .1 % and 9 8 .3 % in CC and TA, r e spe c tive ly ( p> 0 .1 0 ) .
The to tal nymphal mo r tality in CC was 5 2 .6 % ± 2 .5 and
in TA was 5 1 .8 % ± 7 .9 ( ANOVA, F
1 , 1 0= 0 .0 8 , p= 0 .7 7 9 0 ) .
The lo we st mo r tality r ate in CC gr o up was o b se r ve d in the
sec o nd nymphal instar s, and in TA in the fifth nymphal instar s ( Figur e 3 ) . B e fo r e mo ulting to the last nymphal stage , 3 3 .3 %
nymphs die d in CC, while 4 8 .3 % nymphs in the TA gr o up did
no t r e ac h this stage .
The highest mortality rate oc c urred during the fifth stage in
group CC and during the third stage in group TA, when maximum r o o m te m p e r a tur e r e a c h e d 3 1 . 7 ° C a n d h um idity 7 9 % .
Signific antly different mortality between groups was noted in N1 ,
N2 and N5 ( Dunc an test, p< 0 .0 5 ) .
Lo nge vity. The m e an adult sur vival was 1 1 . 9 m o nths ( CC, n = 5 4 ) and 1 6 .2 months ( TA, n = 4 6 ) . Males had a longer
life span, mean survival was 1 2 .9 months and 1 8 .3 months in CC
and TA, respec tively ( ANOVA, F
1 , 1 0 9= 1 0 .4 5 , p = 0 .0 0 1 6 ) . Male
longevity in TA was signific antly higher ( Dunc an test, p< 0 .0 5 ) .
Fecundity– Fer tility. These variables were studied in 2 5 and 2 2 c ouples in CC and TA, respec tively. Fec undity ( H = 0 .0 3 , p =
0 . 8 6 ) and fe r tility ( H = 1 . 5 6 , p = 0 . 2 1 ) value s we r e no t
signific antly different between groups ( Table 2 ) .
Female age at fir st o vipo sitio n was 7 .2 ± 2 .8 days in gr o up
CC and 1 0 .1 ± 4 .6 days in TA ( H = 2 1 .9 4 , p< 0 .0 0 0 1 ) .
Me an numb e r o f e ggs/fe male /we e k ( ANOVA, F
1 ,1 0 1= 4 .4 3 ,
p = 0 .0 3 7 8 ) and numb e r o f r e pr o duc tive we e k s ( F
1 ,4 5= 6 .5 3 ,
p = 0 .0 1 4 1 ) we r e diffe r e nt b e twe e n gr o ups.
40 50 60 70 80 90 100
Jan Feb Mar Ap May Jun Jul Ag Set Oct Nov Dec
Months
H
R
(%)
2000
2001
2002
2003
Fi gu r e 2 - Mon thl y m e an am b i e n t r e l ati ve hu m i di ty f r om Octob e r 2 0 0 0 to Au gu st 2 0 0 3 .
Table 1 - Life cycle of Tr iatoma r ubr ovar ia u n der differen t con dition s of tem peratu re an d relative hu m idity. Corrien tes, Argen tin a. 2000-2003.
Development time*
Age structure CC TA
Mean± SD Mean± SD
Egg 1 5 .6 ± 0 .2 1 9 .1 ± 1 .6
N1 2 6 .5 ± 0 .6 3 4 .8 ± 3 .5
N2 3 1 .9 ± 1 .9 3 9 .0 ± 2 .5
N3 4 1 .6 ± 1 .4 5 9 .5 ± 1 .1
N4 6 7 .7 ± 7 .6 9 1 .2 ± 1 1 .0
N5 1 2 1 .1 ± 1 1 .9 1 9 0 .4 ± 1 7 .0
Duration of cycle egg-adult 3 0 4 .5 ± 1 9 .7 4 3 4 .1 ± 6 .8
* Data expressed in days. SD: standard deviation. CC: controled conditions. TA: ambiental temperature.
0 5 10 15 20 25 30 35 40 45
N1 N2 N3 N4 N5
Nymphal instars
M
o
rta
lity
(%
)
CC
TA
The highest number of eggs/female/week in TA was observed
during the hottest months. A direc t c orrelation between fec undity
and temperature was verified ( r = 0 .5 6 , p< 0 .0 0 1 , n = 2 5 1 ) .
An interruption period of up to six weeks in the oviposition
o c c ur r e d in all the TA fe male s dur ing c o ld as we ll as war m mo nths. This inte r r uptio n was o nly o b se r ve d in 5 CC fe male s
and the lo nge st dur atio n was 3 we e k s. Afte r the inte r r uptio n,
the fe male s c o ntinue d o vipo sitio n until the y die d.
DISCUSSION
Mo st studie s o n life c yc le s in Tr ia to m ina e ha ve b e e n c ar r ie d o ut unde r c o ntr o lle d c o nditio ns o f te mpe r atur e and r e la tive hum idity, a ltho ugh the s e fa c to r s s ho w da ily a nd se aso nal var iatio ns in natur al hab itats1 5.
Al th o u gh n o a s s e s s m e n ts o f th e n a tu r a l b i o to p e o f
T. ru b ro va ri a have been c arried o ut, studies o n mic ro c limatic c o nditio ns within a sim ila r ha b ita ts o f r o c k pile s whe r e
T. b ra silie n sis is found, demonstrated that temperature and relative humidity reaches lower ranges than the external condition ( espec ially on the roc k surfac e)1 4.
Experimental studies revealed that higher temperatures cause a reduction in the developmental period of T. rubrovaria22. Higher
temperature and lower relative humidity also decrease the development time of eggs and nymphs of T. rub ro fa scia ta, T. m e la no so m a,
R. neglectus and R. robustus6 11 18 19. Extremely low humidity can
interrupt the insect development15, although no influence of humidity
on egg development time of R. neglectus was found18.
Although average temperature and relative humidity were s im ila r in th e two e xpe r im e n ta l s itua tio n s un de r wh ic h
T. rub ro va ria were reared, the variability was higher under the ambient c o nditio ns c o mpared with the c o nditio n inside the c limatic c hamber. Room temperature was similar and relative humidity was slightly lower than rec ords obtained within a palm
trees c ommunity in the San Roque department of Corrientes3.
De ve lo pme nt time in the TA gr o up was lo nge r than in the
CC gr o up, c o r r o b o r ating studie s o n the same spe c ie s2 2 and
o n o the r tr iato m ine s, de sc r ib ing lo nge r life c yc le s unde r
c hanging c o nditio ns o f te mpe r atur e and r e lative humidity1 6.
Adult emergenc e in the CC group oc c urred almost all year
long ( February to Dec ember 2 0 0 1 ) at an approximately c onstant
rate, whereas all nymphs of the TA group reac hed the adult stage
between Oc tober and November 2 0 0 1 . In the last experimental group, no rec ruitment oc c urred during the c older months ( April
to September 2 0 0 1 ) .
Sex rate revealed a slight predominanc e of females in the
two experimental groups, suggesting a higher mortality risk
during the preadult develo pment in males, as indic ated fo r
T. i n f e sta n s1 7. Male lo nge vity in the TA gr o up was lo nge r,
c oinc iding with Tria to m a rub ro fa scia ta6.
Changing c onditions of temperature and relative humidity
did not affec t egg survival and total nymphal mortality, as no
differenc e was observed between the two experimental groups. However, the high mortality rate in the third stage in TA oc c urred
during a perio d when the highest temperature and relative
humidity were rec orded. At 3 3 ° C and 7 0 % a c omplete mortality
for Rho dnius ne gle ctus fifth nymphal instars was also reported1 8.
Fe c undity and fe r tility did no t diffe r gr e atly b e twe e n the two experimental gro ups, c o inc iding with the results repo rted
b y Silva2 2 whe n the spe c ie s was k e pt at 2 5 ° C and 3 0 ° C. Date
o f fir st r e pr o duc tio n ( fr o m initial day o f the study) b e gan
e ar lie r in the CC gr o up with highe r var iab ility, as the r e sult o f the lo ng r e c r uitme nt pe r io d to the adult stage in this gr o up.
Constant temperature and humidity were the most optimal conditions for development, the life cycle of T. rubro va ria reared under these conditions was shorter. Although females under room conditions had a longer reproductive period, the number of eggs/ week was lower and oviposition interruptions were c onstantly observed. Developmental time in the group exposed to fluctuating temperature and relative humidity took over a year to complete. As the insects had no food restriction, this might be considered as the species minimum under natural climatic conditions.
This study indicates that fluctuating temperature and humidity h a ve a n i m p o r ta n t e ffe c t o n th e l i fe c yc l e du r a ti o n o f
T. rub ro va ria. A difference of 2 ° C in the mean temperature under whic h the two experimental groups were developed, promoted
c hange s in the life c yc le dur atio n and in the r e pr o duc tive
pe r fo r manc e o f this spe c ie s.
Table 2 - Re produ ctive patte rn s of Tr iato ma r ubr o var ia for e ach grou p te ste d. Corrie n te s, Arge n tin a. 2 0 0 1 -2 0 0 3 .
Groups
CC TA
minimum maximum minimum maximum
( Mean± SD) ( Mean± SD)
Age of first reproduction( data in weeks) 22 63 56 64
( 4 1 .1 ± 1 4 .1 ) ( 6 0 .2 ± 2 .4 )
Eggs/female ( no) 2 1 1 1 3 6 2 4 1 6 1 3 0 1
( 8 1 7 .6 ± 3 3 1 .1 ) ( 8 3 7 .1 ± 2 1 2 .2 )
Reproductive weeks/female ( no) 11 63 20 72
( 3 7 .7 ± 1 4 .2 ) ( 4 9 .3 ± 1 4 .6 )
Eggs/female/week ( no) 1 3 .9 3 0 .7 1 0 .6 3 2 .1
( 2 2 .5 ± 4 .3 ) ( 1 6 .8 ± 4 .2 )
Fertility ( %) 3 0 .9 9 8 .1 2 0 .6 9 3 .7
( 7 5 .1 ± 1 8 .3 ) ( 6 9 .7 ± 1 8 .9 )
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