VECTOR-BORNE AND ZOONOTIC DISEASES
Volume 9, Number 3, 2009
© Mary Ann Liebert, Inc.
DOI: 10.1089/vbz.2008.0078
Variations in Sex Ratio, Feeding, and Fecundity
of Triatoma dimidiata (Hemiptera: Reduviidae)
Among Habitats in the Yucatan Peninsula, Mexico
V. Payet,1,2 M. J. Ramirez-Sierra,1 J. Rabinovich,3 F. Menu,2 and E. Dumonteil1,4
Abstract
Chagas’ disease is a major public health concern in most Latin American countries and its prevention is based
on insect vector control. Previous work showed that in the Yucatan peninsula of Mexico, houses are transiently
infested by adult Triatoma dimidiata, which then fail to establish sustained colonies. The present study was designed to evaluate the seasonality and possible causes of the dispersal of sylvatic T. dimidiata toward the houses
and the subsequent failure of colonization. Dispersal was highly seasonal and correlated with temperature,
pressure, and wind speed. Analysis of sex ratio, feeding status, and fecundity of sylvatic populations of T.
dimidiata indicated a rather low feeding status and low potential fecundity, suggesting that seasonal dispersal
may be associated with foraging for better conditions. Also, feeding status and potential fecundity tended to
improve in the domestic habitat but remained largely suboptimal, suggesting that these factors may contribute to the ineffective colonization of this habitat.
Key Words: Chagas’ disease—Triatomine—infestation—population dynamics.
Introduction
C
hagas’ disease, caused by the protozoan parasite Trypanosoma cruzi, is a major public health concern in most
of Latin America. It is transmitted to humans primarily by
domiciliated hematophagous triatomine vectors (Hemiptera:
Reduviidae). However, some vector species are not strictly
domiciliated and show varying levels of adaptation to human dwellings. For example, we previously showed that in
the Yucatan peninsula of Mexico, houses in both rural and
urban areas are transiently infested during the months of
April–July by adult Triatoma dimidiata, but these invading
bugs have only a limited ability to establish sustained
colonies in the domiciles (Dumonteil et al. 2002, 2007, Guzman-Tapia et al. 2007).
T. dimidiata is a major Chagas’ disease vector distributed
from central Mexico to northern Colombia and Venezuela,
and through most of central America (Dorn et al. 2007). It
actually includes several cryptic species distributed in specific geographic areas (Panzera et al. 2006), and this genetic
diversity has major implications in terms of vector ecology,
behavior, and epidemiological importance (Bargues et al.
2002, Dorn et al. 2007, Panzera et al. 2006). T. dimidiata thus
seems to be a domiciliated vector in most of Central America and central Mexico, whereas it is rather sylvatic in the
southeast of Mexico, Belize, and some parts of Guatemala.
These non-domiciliated vector species require novel control
strategies to efficiently control Chagas’ disease transmission,
and this represents an important challenge for public health.
Indeed, we showed that conventional indoor insecticide
spraying eliminates domestic T. dimidiata populations for
only a short time, presumably because reinfestation from sylvatic bugs occurs rapidly (Dumonteil et al. 2004). Furthermore, using mathematical modeling, we have shown that although dispersal of sylvatic bugs is key to explaining T.
dimidiata domestic population dynamics in Yucatan, this dispersal is not sufficient, and very low fertility and survival of
domestic populations are also required (Gourbière et al.
2008). Taken together, these studies indicate that it is of key
importance to understand further which factors may con-
1Laboratorio de Parasitología, Centro de Investigaciones Regionales “Dr. Hideyo Noguchi,” Universidad Autónoma de Yucatán, Mérida,
Mexico.
2Laboratoire de Biométrie et Biologie Evolutive, UMR CNRS 5558, Université Claude Bernard Lyon 1, Université de Lyon, Villeurbanne,
France.
3Centro de Estudios Parasitológicos y de Vectores, Universidad Nacional de La Plata, La Plata, Argentina.
4Department of Tropical Medicine, Tulane University, School of Public Health and Tropical Medicine, New Orleans, Louisiana.
243
244
tribute to the dispersal of sylvatic bugs toward the houses,
and their subsequent failure to establish a sustained colonization, as this understanding may allow optimization of
vector control strategies.
Dispersal of triatomines is usually associated with foraging for feeding and/or mating (Forattini 1980), and environmental conditions, population density and nutritional
status, and sex are well-established factors influencing dispersal. For example, warmer temperatures, low winds, and
low nutritional status favor T. infestans dispersal (Ceballos et
al. 2005, Galvao et al. 2001, Lehane et al. 1992, VazquezProkopec et al. 2004, 2006), and females disperse more than
males (Gurevitz et al. 2006, 2007, Schofield et al. 1992). Similarly, unfed female T. guasayana disperse preferentially
(Wisnivesky-Colli et al. 1993). In contrast, starving T. pseudomaculata and T. brasiliensis of both sexes were found to disperse during the dry season (November), possibly in search
for food sources (Carbajal de la Fuente et al. 2007). In the
case of T. dimidiata, dispersal has been observed during the
hot and dry season (Dumonteil et al. 2002, Monroy et al.
2003b). Also, males have been reported to disperse more than
females in Guatemala and Costa Rica (Monroy et al. 2003a,
2003b), but more females than males infest houses in the Yucatan peninsula, Mexico (Dumonteil et al. 2002).
Domiciliation, on the other hand, has been proposed to result from either a gradual adaptation to the domestic environment through selection, or a response to reduced availability of feeding sources and/or perturbation of the natural
habitat, and its success depends on the ability of the infesting bugs to find appropriate blood sources and refuges for
reproduction inside the houses (Forattini 1980, Schofield et
al. 1999). Colonization may be favored by the arrival of
gravid females in the houses (Schofield et al. 1999, Carbajal
de la Fuente et al. 2007).
As a first approach to understanding these aspects of T.
dimidiata population dynamics and house infestation, we investigated the variations in climatic conditions, sex ratio,
feeding status, and fecundity of bugs from natural populations in the Yucatan peninsula of Mexico.
Material and Methods
Triatomine collection
Domestic and peridomestic triatomines were collected
from 38 rural villages in the Yucatan peninsula, Mexico, by
community participation during the years 2000, 2001, 2003,
and 2004, as previously described (Dumonteil and Gourbière
2004, Dumonteil et al. 2002, Guzman-Tapia et al. 2005).
Briefly, households were instructed to collect any triatomine
found inside their house (domestic) or yard (peridomestic)
in separate plastic vials, using a plastic bag or a sheet of paper to avoid direct skin contact with the bugs. Triatomines
were then gathered during weekly to monthly visits to the
villages. To allow for year-to-year comparison, the same collection effort was exerted each year (no collections could be
performed during 2002 for logistical constraints). Sylvatic
bugs were collected by manual collection from a single sylvatic spot located about 1.5 km away from the village of Tetiz
for 17 consecutive and nonconsecutive nights during the
months of May–July 2003 and 2004. Briefly, two trained researchers collected bugs moving toward them at nightfall
(7–10 pm), using flashlights to locate the approaching tri-
PAYET ET AL.
atomines. Additional sylvatic bugs were collected by hunters
from the study villages using the same technique (March–
June 2000, 2001, and 2003). All bugs were taken to the laboratory for processing and analysis.
Meteorological data
Monthly data sets for average temperature, precipitation,
ground level atmospheric pressure, relative humidity, zonal
winds (flowing along the latitude), and meridional winds
(flowing along a meridian) were obtained from the National
Oceanic and Atmospheric Administration–Cooperative Institute for Research in Environmental Sciences Climate Diagnostics Center (Boulder, CO) (http://www.cdc.noaa.gov/),
for the periods corresponding to the field bug collections
(Kalnay et al. 1996). Field data for temperature, precipitation,
and wind speed, recorded every 15 min in a nearby village
(Hunucma, 5 km away) by an automatic weather station,
were obtained from the Servicio Meteorológico Nacional of
Mexico. Average data were calculated from these records for
the days and time periods (7–10 p.m.) corresponding to the
manual collection of sylvatic bugs.
Population genetics
Assignment tests based on genetic data have been used
(Dumonteil et al. 2007) to identify insects that were possible
migrants from a different biotope than that in which they
had been collected. Assignments based on four microsatellite markers were performed by likelihood and Bayesian
methods (Dumonteil et al. 2007). The likelihood method uses
allelic frequencies in each population in order to calculate
the likelihood that a given genotype belongs to a certain population. If an individual genotype is more likely to belong to
a population other than that from which it was sampled, the
individual is considered a migrant (Schneider et al. 2001).
The Bayesian approach was used to calculate the probability that a given genotype belonged to a particular population using a Monte Carlo re-sampling procedure that simulated a large number of random multilocus genotypes based
on allele frequencies directly estimated from the reference
population samples (Cornuet et al. 1999). We looked at the
sex ratio of migrants identified by the different methods from
both the peridomestic and sylvatic habitats and compared it
to the sex ratio in the populations of origin to identify potential differences in dispersal between sexes.
Feeding status
Fresh weight was used as an indicator of feeding status of
subsets of the collected bugs (Ceballos et al. 2005, Noireau
and Dujardin 2001). For this analysis, only live specimens
brought to the laboratory within 2 days of their collection in
the field were used (n 50) and weighed (0.1 mg precision).
In addition, fully fed status was estimated by allowing a random subset of field-collected bugs (n 15) to feed on pigeons for 30 min in the dark, and weighing them immediately after feeding. These fully fed bugs were then kept in
the laboratory at constant temperature (25°C) for up to 3
weeks and weighed at various time points to determine the
rate of weight loss following feeding. The potential duration
of fasting of the field-collected bugs was estimated by nonlinear interpolation of weight loss over time.
Triatoma dimidiata BIOLOGY IN MEXICO
245
Reproductive status
Results
Subsets of collected female bugs were dissected and the
number of eggs in their ovaries was counted as an indicator
of reproductive status and/or of potential fecundity (Lopez
et al. 1999). From these dissections, we determined separately the proportion of females with eggs and, for females
with eggs, the number of eggs per female, as well as the average number of eggs per female.
Seasonal climatic variations and T. dimidiata populations
Data analysis
Data are presented as proportions, mean SD, or box
plots. Because of the reproducibility of the seasonal pattern
observed (see Results), data from all the years of field collections were pooled by trimester (January–March; April–
June; July–September; October–December) for analysis of
seasonal variations as well as for comparisons of triatomine
sex ratio, potential fecundity, or feeding status between
biotopes. Proportion data were analyzed by the ␹2 test or
Fisher’s exact test. Because of departures from normality
and/or unequal variances, weight data and egg counts were
analyzed by the Kruskal-Wallis test, and when significant,
by Dunn’s multiple comparisons post-hoc test. Standard correlation analysis was performed to assess the potential relationships between bug collections and climate parameters.
All statistical analysis were performed with JMP 5.0 software
(Sall et al. 2004).
To detect a possible relationship between house infestation by T. dimidiata in the Yucatan and climate variations, we
looked at the seasonal variations in meteorological parameters and domestic bug abundance over 4 years of field collections. In spite of some year-to-year variation, there was a
clear annual pattern of a sharp increase in domestic bug
abundance during the months of April–June, followed by a
more progressive decrease in the months of July–December
(Fig. 1A). The consistency and reproducibility of this pattern
during this time-series confirmed the seasonality of the infestation process and T. dimidiata dispersal described previously (Dumonteil et al. 2002, 2007). Bug abundance was significantly correlated with monthly average humidity (r2 0.277, P 0.036), mean temperature (r2 0.283, P 0.034),
ground level atmospheric pressure (r2 0.439, P 0.005),
zonal wind (r2 0.461, P 0.003), and meridional wind
(r2 0.537, P 0.001) (Fig 1B). A multivariate regression
model provided an excellent fit of bug abundance data with
only three significant climate parameters: temperature, pressure, and zonal wind (r2 0.884, F 30.51, P 0.0001). We
further evaluated the possible relationships between the
number of sylvatic bugs collected each night during
May–July and the average field climate data during these
nights (7–10 p.m. average). A total of 50 sylvatic bugs were
collected manually during 17 nights of fieldwork (2.9 1.9
FIG. 1. Time-series of domestic T. dimidiata abundance and seasonal variations in three climatic variables. The total numbers of T. dimidiata collected in the domiciles is shown as a function of time during 4 years (A). The corresponding variations in pressure, mean temperature, and zonal wind (B) were significantly correlated with bug abundance: mean temperature (r2 0.283, P 0.034), pressure (r2 0.439, P 0.005), zonal wind (r2 0.461, P 0.003). The gray shaded areas
indicate the period of April–June (A–J).
246
Table 1.
PAYET ET AL.
Seasonal Variations in T. dimidiata Sex-Ratio (% females/(males females)) in Diffferent Habitats
January–
March
April–June
48.6%
(88/181)
50.0% (33/66)
65.9%b,c
(735/1076)
59.9% (94/157)
49.7%
(165/332)
54.7%
(270/493)
Trimester
Domestic
Peridomestic
Sylvatic
July–
September
October–
December
65.1%
(239/367)
63.8%
(83/130)
ND
68.1a (47/69)
57.4% (35/61)
ND
difference in sex ratio with the January–March trimester (Fisher’s exact test, P 0.0001).
difference in sex ratio with the sylvatic habitat (Fisher’s exact test, P 0.0001).
cSignificant difference in sex ratio with the peridomestic habitat (Fisher’s exact test, P 0.045).
aSignificant
bSignificant
bugs/night). However, no significant correlation was observed between the number of collected bugs per night and
any of the climate parameters analyzed, although no lag correlation was tested. Attempts were also made to collect sylvatic triatomines during additional periods of the year, but
too few bugs were collected for analysis.
based on microsatellite markers (Dumonteil et al. 2007). Both
methods of assignment suggested that the sex ratio of migrants from peridomestic and sylvatic areas may be biased
toward females in comparison with the sex ratio observed
in these habitats, but this trend was statistically significant
only for sylvatic migrants identified by Bayesian assignment
(Fisher’s exact test P 0.041; Table 2).
Variations in sex ratio of T. dimidiata populations
We compared the sex ratio of bugs collected in different
habitats and evaluated the seasonal variation. No significant
seasonal variations in sex ratio were detected in bugs collected in the peridomestic habitat, in spite of a slight increase
in the proportion of females in July–September (␹2 3.58,
P 0.31) (Table 1). In the sylvatic habitat, the sex ratio remained constant during first two trimesters, with a proportion of females around 50% or slightly higher (␹2 2.04, P 0.15), but no reliable estimates of the sex ratio could be made
for the remainder of the year because of the very low number of bugs collected. In contrast, in the domestic habitat, we
observed a significant increase in the proportion of females
starting in the April–June trimester (␹2 25.6, P 0.0001),
and this high proportion of females was maintained during
the rest of year (Table 1). The proportion of females in the
domestic habitat during the April–June trimester was also
significantly higher than that observed in the peridomestic
or sylvatic habitats (Fisher’s exact test, P 0.045 and P 0.0001, respectively). Taken together, these data suggested
that during the April–June trimester there was either a preferential dispersal of female sylvatic bugs toward the domiciles or a higher mortality of males in the domestic area. To
further assess these possibilities, we looked at the sex of potential migrant triatomines identified by assignment tests
Variations in feeding status of T. dimidiata populations
We used body weight as a first approximation of nutritional and energetic status of bugs collected in different
biotopes during the months of May–July (Ceballos et al. 2005,
Noireau and Dujardin 2001). At this time of the year, both
female and male sylvatic bugs were poorly fed when compared to fully fed insects (for both sexes, P 0.001, Dunn’s
multiple comparison test) (Fig. 2A and B). Indeed, their blood
meals represented only 41% and 45% of a full blood meal for
females and males, respectively. Domestic bugs seemed to
present a slightly better feeding status than sylvatic bugs,
but this difference did not reach statistical significance, and
their overall feeding level was about 50% and 67% of that of
fully fed females and males, respectively (Fig. 2A and B).
Nonetheless, a few domestic bugs seemed able to achieve
nearly full feeding status as indicated by the wide distribution of fresh weights (Fig. 2A and B). Taken together, these
data indicate a partial feeding by natural populations in both
habitats. Alternatively, these findings may indicate prolonged fasting following a complete meal. Monitoring the
rate of weight loss following a full blood meal in the laboratory suggested that domestic bugs may have been fasting
for up to 10 to over 20 days, and sylvatic bugs for over 18
days (Fig. 2C).
Table 2. Comparative Sex Ratio in Different Habitats and Among
Migrant Triatomines Identified through Distinct Methods
Biotope
Peridomicile
Sylvatic
Field
Migrants
(likelihood
assignment)
Migrants
(Bayesian assignment)
59% (245/414)
52% (435/825)
66% (2/3)*
86% (6/7)a
100% (2/2)**
100% (5/5)b
Data are presented as % females (females/(males females)).
aP 0.08 and bP 0.04 using Fischer’s exact test versus field sex ratio.
Triatoma dimidiata BIOLOGY IN MEXICO
247
FIG. 2. Feeding status of T. dimidiata from different habitats. Female (A) and male (B) live insects were weighed within
2 days of capture in domestic or sylvatic habitats during the months of May–July (n 50). A random subset of bugs (n 15) was allowed to feed on pigeons in the laboratory to estimate fully fed status. Weights were significantly different for
both females and males from the different groups (Kruskal-Wallis 20.53 and 14.14, respectively, P 0.001); the asterisks
indicate a significant difference between the weight of bugs from the indicated groups (Dunn’s multiple comparison tests,
P 0.01 and P 0.001, respectively). (C) Kinetics of weight loss following full feeding of female and male triatomines.
Variations in potential fecundity in T. dimidiata populations
We determined the proportion of females with eggs and,
for females with eggs, the number of eggs per female in bugs
from the different habitats, as an indicator of their potential
fecundity (Lopez et al. 1999). For the period April–June, we
observed that over 25% of sylvatic females had eggs, whereas
this was the case in 12%–13% of peridomestic or domestic
females (Fig. 3A; ␹2 13.8, d.f. 2, P 0.001). However,
sylvatic bugs had less than half the number of eggs per female as bugs from the domestic or peridomestic habitat
(overall, 0.85 0.33 eggs versus 2.12 0.48 or 1.45 0.36
eggs, respectively) (Fig. 3B; Kuskal-Wallis 19.24, P 0.001, Dunn’s test P 0.05), and the maximum number of
eggs found in sylvatic bugs was also less than half of that
from bugs from domestic and peridomestic habitats. Taken
together, these data indicate that during this trimester, females from the sylvatic habitat had a lower mean potential
fecundity compared to bugs from the peridomestic or domestic habitat. There was a weak but significant correlation
between female weight, i.e., their blood meal size, and egg
content (r2 0.33, P 0.008). We also assessed possible seasonal variations in the potential fecundity of females in the
domestic habitat. A slightly higher proportion of females had
FIG. 3. Potential fecundity of females from different habitats during May–July. (A) Proportion of female bugs with eggs.
Numbers above the bars indicate the actual number of females with eggs and the total number of analyzed bugs. (B) Box
plot of the number of eggs per females calculated from all the females with eggs. An asterisk indicates a significant difference between bugs from different habitats [␹2 13.8, d.f. 2, P 0.001 in (A) and Kuskal-Wallis 19.24, P 0.001, Dunn’s
test P 0.05 in (B)].
248
eggs in the last two trimesters of the year (July–September
and October–December) than in the first two trimesters (January–March and April–June), but this difference was not statistically significant (Fig. 4A; ␹2 7.5, d.f. 2, P 0.056),
and egg number per female remained constant (Fig. 4B;
Kruskal-Wallis 2.12, P 0.55), suggesting little seasonal
variation in egg production and the potential fecundity of
domestic females during the year.
Discussion
The present study represents a first attempt at identifying
some of the factors that may contribute to the dispersal of
sylvatic T. dimidiata bugs toward houses and their subsequent failure to establish sustained colonization in the domiciles. Our data from several years of field collections unambiguously confirmed that there is a very regular and
reproducible seasonal infestation of the domiciles by T.
dimidiata in the Yucatán. Together with our previous field
studies (Dumonteil et al. 2002), population genetics studies
(Dumonteil et al. 2007), and modeling studies (Gourbière et
al. 2008), these observations also confirm that dispersal is a
seasonal process. Unsurprisingly, this pattern was correlated
with seasonal climate variations, in agreement with observations on the dispersal of T. infestans (Carbajal de la Fuente
et al. 2007, Gurevitz et al. 2006, Schofield et al. 1992, VazquezProkopec et al. 2004, 2006). Interestingly, stronger winds
seem to limit T. infestans active dispersal (Vazquez-Prokopec
et al. 2006), whereas our data suggest that they are associated with a maximum dispersal of T. dimidiata. Nevertheless,
we did not observe any association between dispersal of sylvatic T. dimidiata and climatic conditions at the time of dispersal. These data suggest that dispersal may be associated
with specific seasonal climatic conditions, but the trigger for
dispersal may be independent of the prevailing climatic conditions immediately before or during flight, and may rather
depend on endogenous factors such as physiological status
and/or activity rhythm, or on an interaction between those
factors and climatic conditions.
PAYET ET AL.
As a first step toward understanding this process, we further assessed sex ratio, feeding and reproductive status of T.
dimidiata, and their variations according to habitat and seasons, as these factors have been shown previously to greatly
influence triatomine dispersal as well as the success of the
colonization process (Ceballos et al. 2005, Forattini 1980, Galvao et al. 2001, Lehane et al. 1992, Vazquez-Prokopec et al.
2004, 2006). The difference in sex ratio between domestic and
sylvatic bug populations, as well as the seasonal increase in
females infesting houses, further suggest that females may
preferentially disperse and arrive in the houses. This seemed
confirmed by the observation that migrant bugs identified
by microsatellite markers tended to be predominantly females, but a larger sample size would be required to reach
a definitive conclusion. A greater dispersal ability has been
reported in female triatomines from other species such as T.
infestans, T. guasayana, or T. rickmani (Galvao et al. 2001, Gurevitz et al. 2007, Monroy et al. 2004, Schofield et al. 1992, Wisnivesky-Colli et al. 1993). However, in the case of T. dimidiata, previous studies in Costa Rica and Guatemala reported
a male-biased sex ratio in infested houses, suggesting that
males had better dispersal abilities (Monroy et al. 2003a).
These discrepancies may be related to the distinct taxonomic
status of the different populations of T. dimidiata in the Yucatan and Central America, and they may indicate further
behavioral differences between the cryptic species identified
(Dorn et al. 2007). Finally, the preferential infestation of
houses by T. dimidiata females should favor colonization, as
these bugs may rapidly lay eggs if they find appropriate
feeding sources, mates, and refuges (Carbajal de la Fuente et
al. 2007, Forattini 1980).
Our data on feeding status show that both sylvatic and
domestic bugs collected at the time of dispersal (April–June)
had rather small blood meals, indicating either recent but
very incomplete feeding (at best 67% of a full blood meal),
or prolonged fasting of over 2 weeks following a full meal.
Natural feeding rates and amounts of blood ingested are unknown for T. dimidiata, but estimates for T. infestans are much
higher, with feeding every 1–10 days; furthermore, even
FIG. 4. Yearly variations in potential fecundity of females from domestic habitat. (A) Proportion of females with eggs.
Numbers above the bars indicate the actual number of females with eggs and the total number of analyzed bugs. The slight
increase in the proportion of females with eggs did not reach statistical significance (␹2 7.5, d.f. 2, P 0.056). (B) Box
plot of the number of eggs per female. There were no significant variations during the year (Kruskal-Wallis 2.12, P 0.55).
Triatoma dimidiata BIOLOGY IN MEXICO
though incomplete feeding is frequent, T. infestans seems able
to achieve fuller blood meals (Canals et al. 1999, Lopez et al.
1999). Thus, T. dimidiata feeding may be considered relatively
poor in both habitats and the search for blood sources may
be a key contributing factor for their dispersal. Dispersal of
triatomines has indeed been shown to be dependant on feeding status (Ceballos et al. 2005, Galvao et al. 2001, Lehane et
al. 1992, Vazquez-Prokopec et al. 2006, Wisnivesky-Colli et
al. 1993), and a preferential dispersal of females may be due
to greater energetic requirements to support ovogenesis. Indeed, T. phyllosoma females require almost twice as much
blood as males, and they dedicate about 66% of their energy
budget to egg production (Collier et al. 1977). In contrast, T.
dimidiata females require about 30% more blood than males
(Zeledón 1981). Furthermore, because of the seasonality of
dispersal we observed in the case of T. dimidiata, it is possible that a reduction in sylvatic blood sources availability may
occur during the months of active dispersal. However, no
data to support this hypothesis are available on the population dynamics of potential sylvatic mammalian hosts in the
region. In addition, attempts were made to collect sylvatic
bugs during additional periods of the year, but very few
were collected, suggesting that sylvatic bugs may not disperse much outside the April–June period and remain hidden.
Interestingly, the slightly improved feeding status of domestic bugs compared to that of sylvatic ones seems counterintuitive because active dispersal in triatomines is very energy-consuming and results in major weight loss in T.
infestans (Schofield et al. 1991). This suggests that in spite of
this initial weight loss, at least a small proportion of domestic
bugs may be able to find sufficient blood sources in the human dwellings to reach a nutritional status better than their
pre-dispersal one. Finally, small blood meal size delays defecation and reduces feces volume in T. infestans (Kirk and
Schofield 1987, Trumper and Gorla 1991); a similar effect in
T. dimidiata would result in a lower T. cruzi transmission risk
to humans and other hosts.
Egg counts, used as an indicator of potential fecundity
(Lopez et al. 1999), revealed that egg production of domestic females was almost half that of laboratory colonies of T.
dimidiata (18 16 versus 30 15 eggs/female, respectively)
(Guzmán-Marín et al. 1992, Zeledón 1981), and egg production was even lower for sylvatic bugs. Two factors have been
found to greatly contribute to egg production in triatomines:
mating and nutritional status (Collier et al. 1977, Lopez et al.
1999, Zeledón 1981). Indeed, in T. infestans, virgin females
have been found to produce fewer eggs than mated females
(Lopez et al. 1999). Mating status was not investigated here.
However, in natural populations of T. infestans, the majority
of females are mated (Lopez et al. 1999). Also, a single copulation is enough to allow T. dimidiata females to produce
fertile eggs for most of their life span (Zeledón 1981). Mating may thus play only a minor role in explaining the observed variations in egg production.
Egg production appeared to match closely feeding status:
the slightly better fed domestic bugs showed about twice as
many eggs per female as sylvatic bugs, but this remained
suboptimal compared to laboratory-raised females. These
data are in agreement with the important and constant energetic requirement for egg production in triatomines (Collier et al. 1977, Zeledón 1981). For example, blood meals of
249
R. prolixus need to represent at least 31% of a full meal to initiate egg production (Friend et al. 1965). Assuming a similar
threshold for T. dimidiata, only 63 mg and 90 mg of blood
would be available for egg production for sylvatic and domestic females, respectively. Based on blood requirements
of 10 mg blood/egg (Zeledón 1981), T. dimidiata females
would be expected to be able to produce about 6.3 and 9 eggs
in sylvatic and domestic habitats, respectively, which approximately matches our observed data.
Taken together, our data suggest that a limited potential
fecundity resulting from poor feeding of domestic T. dimidata may contribute to its failure to effectively colonize
houses. Furthermore, if the poor feeding we observed in
adults is also indicative of poor feeding of larval stages inside the houses, it may result in limited development
and/or high mortality of larval stages. Indeed, feeding
sources influence development times of triatomines
(Guarneri et al. 2000a, 2000b), and incomplete blood meals
may interfere with molting or extend the duration of larval
stages, as well as adult fecundity, as observed for R. prolixus (Friend et al. 1965, Patterson 1979). These observations
are in good agreement with a theoretical model that predicted that a very low fertility of adults and a low survival
of larval stages were required in the domestic habitat to fit
the observed population dynamics pattern of T. dimidiata
in the Yucatan (Gourbière et al. 2008). Finally, suboptimal
feeding and potential fecundity in the domestic habitat
(compared to fully fed insects) may also explain why bugs
dispersing from the houses to the peridomicile and even
the sylvatic habitat have been detected (Dumonteil et al.
2007), and foraging for better feeding sources may contribute to the bugs’ leaving the domestic habitat. This seems
counterintuitive, as houses are believed to provide abundant and stable blood meal sources, leading to effective colonization of this habitat. Further studies should help understand why triatomines are unable to improve their
feeding status inside the houses.
In conclusion, our study of T. dimidiata feeding and fecundity in natural populations suggests that the seasonal dispersal of sylvatic bugs to the houses may be related to their
greater foraging activity in search for blood sources. This seasonal dispersal was well correlated with seasonal climatic
variations, but it may instead be triggered by daily physiological status. Furthermore, in spite of a female-biased house
infestation, which should favor colonization, suboptimal
feeding inside the houses as well as suboptimal potential fecundity may contribute to poor colonization of the domiciles.
Additional studies on feeding sources, mating, and reproductive success should help confirm these hypotheses and
may provide additional clues for the optimization of vector
control strategies.
Acknowledgments
This study was funded by grant no. 20020404 from
SISIERRA/CONACYT, Mexico, to E.D.; by grant no. 03 00
57 3401 from the Région Rhône-Alpes, France, to V.P. and
F.M.; and by the program “Action des coopérations scientifiques avec l’Argentine” ECOS SUD (A04B02, Resp. C.
Bernstein) to F.M and J.R. We thank M. Euan-García and L.
Chavez-Nuñez for technical assistance and J. García-Rejon
for helpful discussions on the manuscript.
250
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Address correspondence to:
Dr. Eric Dumonteil
Laboratorio de Parasitología
Centro de Investigaciones Regionales “Dr. Hideyo Noguchi”
Universidad Autónoma de Yucatán
Ave. Itzaes #490 x 59
97000 Mérida, Yucatán
Mexico
E-mail: [email protected]