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Keywords:

  • Blood consumption index;
  • blood meal;
  • food resource use;
  • reproductive parameters;
  • triatomine

ABSTRACT:

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

Triatoma patagonica (Del Ponte, 1929) (Hemiptera-Reduviidae) is a peridomestic vector of Chagas disease that has been frequently found colonizing peridomestic structures in several localities in Argentina. Studying relationships between feeding and reproductive factors is important because these traits regulate population density and define vectorial capacity. Since T. patagonica can circulate among peridomestic structures taking blood from both bird and mammal hosts, we evaluated the extent to which different blood meal sources affect food resource use and reproductive parameters. We used 5th instar nymphs and females that fed on either guinea pigs or pigeons to estimate food resource use. We estimated reproductive parameters in adults that fed on these sources. Nymphs and adults showed differences in blood consumption between feeding sources. Females fed on pigeons ingested more blood and needed a higher amount of blood to produce an egg than females fed on guinea pigs. There were no differences in the number of eggs laid and hatched between insects fed on different feeding sources. The higher amount of blood ingested and consumed by T. patagonica fed on pigeons did not translate into higher fecundity or fertility. The lower amount of guinea pig blood ingested was offset by its high nutritional quality.


INTRODUCTION

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

Triatoma patagonica is a peridomestic vector of Chagas disease that has been found colonizing domiciles and most commonly peridomiciliary structures in different Argentine provinces (Lent and Wigodzinsky 1979, Ferrero et al. 1999, Wisnivesky-Colli et al. 2003, Giraldez et al. 2009). Several factors define the competence of a triatomine as a vector of Chagas disease, such as reproductive characteristics and the relationship with feeding-related patterns. In triatomines, blood feeding is used to obtain the resources necessary for female reproduction and for this reason, blood consumption and ovarian development are physiologically integrated (Catalá de Montenegro 1989, Lehane 1991). Intakes per se do not define the nutritional needs of a triatomine or how much ingested blood contributes to fecundity (Montenegro and Passina 1984). Accordingly, blood consumption constitutes an important indicator of the amount of ingested blood that is converted into body substance. The importance of and the relationship between feeding and reproductive factors are well known for several triatomine species (Brasileiro 1982, Catalá de Montenegro 1983, Cabello et al. 1987, Lima et al. 1987, Guarneri et al. 2000, Pires et al. 2004). For T. patagonica, there is information on feeding and defecation patterns in nymphs and adults (Nattero et al. 2002, Rodriguez et al. 2009), however, feeding patterns and the use of blood ingested have still not been explored in terms of reproductive parameters.

In triatomines, blood meal size may be affected by different environmental (temperature) and physiological (age of the insect, gonadotrophic cycle status, previous history of food, and food source) factors (Catalá de Montenegro 1989, Lehane 1991, Catalá et al. 1992). Blood meal source has been considered an important factor affecting nymphal development and mortality as well as reproductive parameters related to the adaptation to different host-feeding preferences of each species, among other factors (Braga et al. 1999, Guarneri et al. 2000, Emmanuelle-Manchado et al. 2002, Martínez-Ibarra et al. 2003). These differences can be attributed to the environment where they live and to the natural history of each species (Cabello et al. 1987, Guarneri et al. 2000). On the other hand, fecundity and fertility may be affected by factors such as age, nutritional status, and the number of copulations (Rabinovich 1985, Guarneri et al. 2000, Pires et al. 2004, Daflon-Teixeira et al. 2009, Nattero et al. 2011). Fecundity is affected by feeding frequency because, to lay eggs regularly, a female needs to eat frequently (Davey 1967, Stoka et al. 1987). Furthermore, the amount of blood remaining in the stomach from the last larval meal conditions the first oviposition (Noriega 1992). Therefore, those females that carry over large nutritional reserves from 5th instar nymphs would ensure the first cycle of egg production in the absence of blood intake during the adult stage (Da Silva Cunha and Ferreira Brasileiro 1988, Davey 2007). This phenomenon, known as autogeny, has been described for several triatomine species (Zeledón et al. 1970, Noriega 1992) and also for T. patagonica (Carrizo et al. 2003) and shows the importance of studies involving food resource use in the last nymphal stage in autogenic triatomine species.

Knowing feeding dynamics and reproduction efficiency in triatomines is important because feeding and food resource use, which have a direct effect on the developmental time of nymphs and adult reproduction, are among the main factors regulating population density (Schofield 1980, 1982). Moreover, feeding and reproductive characteristics determine the ability of a species to become established after the introduction of some individuals into a new habitat (Carey 2001).

Peridomestic triatomine species can circulate among different peridomestic structures, feeding on both bird and mammal domestic hosts. In this research we studied the extent to which different blood meal sources affect reproductive parameters and the use of food resources in Triatoma patagonica. This species is in the process of adapting to human dwellings in accordance with their biological characteristics, including life cycle, reproduction and antennal phenotype (Rodríguez 20111, Rodríguez et al. 2013). It is also adapting to a wide geographic range where this species has been reported colonizing the peridomiciliary structures in Argentina (Lent and Wigodzinsky 1979, Virla de Arguello 1984, Ferrero et al. 1999, Wisnivesky-Colli 2003). We specifically evaluated whether the blood meal source influences: 1) the use of food resources and the conversion of ingested blood into body components in the last nymphal instar and female adult, 2) the amount of blood ingested and its relationship with fecundity, and 3) reproductive parameters and life span in females.

MATERIALS AND METHODS

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

Insects

Sixty 4th and 5th instar T. patagonica nymphs were supplied by the Coordinación Nacional de Control de Vectores (Córdoba, Argentina) from a third-generation colony collected from peridomestic structures from Avellaneda, Río Negro province, Argentina. During all the experiments, insects were kept in the laboratory at 26 ± 2º C, 60–70% RH and a photoperiod of 12:12 h (L:D). Bugs were fed regularly every 15 days on pigeon, Columba livia, until molting.

New 5th instar nymphs were used in experiments of food intake and resource use. When 5th instar nymphs molted to the adult stage, they were used to determine food resource use and conversion efficiency of blood intake into body substances, as well as to estimate reproductive parameters.

Food resource use

All experiments were performed for two food sources: pigeon (C. livia) and guinea pig (Cavia porcellus). Five pigeons that were from no more than one year in the laboratory and four guinea pigs less than one-year-old were used. While the bugs fed, the pigeons were immobilized and the guinea pigs were placed in small plastic cases. For each assay, no more than five bugs were used and were allowed to feed ad libitum until the bug itself removed its proboscis without trying to probe again. To estimate the blood consumption index and the efficiency of conversion of ingested blood into body substance for each insect, it was necessary to determine the food reserve contained in the stomach based on external variables. For this purpose, we followed the method proposed by Giojalas and Catalá de Montenegro (1987) for 5th instar nymphs and by Catalá de Montenegro (1983) for adults. In both cases, this methodology is based on the functional relationship between the weight of the stomach and the weight of the insect. For these estimations, bugs were fed ad libitum within seven days after ecdysis. In order to obtain variability in blood content in the stomach, bugs were sacrificed at 0, 5, 10, and 15 days post-ingestion. At the time of sacrifice, we recorded the weights of the stomach and the insect. With these data, we estimated the amount of blood contained in the stomach (BCS), regressing the weight of the insect and the weight of the stomach. For the 5th instar nymphs, the linear regression obtained was BCS =−23.41 + 0.61x, R2= 0.91. For females, the linear regression obtained was BCS =−14.07 + 0.32x, R2= 0.71. In both cases, the linear regression showed a significant association (p<0.001). These equations were then used in the estimations that are described below. We used 21 and 25 5th instar nymphs and adults, respectively, to define this equation.

Estimations of blood consumption index and efficiency of conversion of ingested blood for 5th instar nymphs and females

For these estimations, we followed the method proposed by Catalá et al. (1992) for blood consumption index (CI) and by Montenegro and Pasina (1984) for the efficiency of conversion of ingested blood. During the experimental period (ten days), each bug was offered food twice. To calculate the CI and the efficiency of conversion of ingested blood (ECB), we recorded the individual mean weight daily and on each feeding event, the amount of blood intake. The CI is a measure of the blood consumed per day in milligrams and was calculated as CI= ((Bi + F) – Be)/ T, where Bi is the blood contained in the stomach at the start of the experiment (estimated from the equation described above), F= weight of ingested food (sum of intakes), Be= blood contained in the stomach at the end of the experiment, and T= duration of experimental period (in days).

ECB was also used to indicate the percentage of ingested blood converted into body substance and was calculated as ECB= G + DP / (Bi + F) – Be, where G = weight gained during the experimental period (difference in weight at the end and beginning of the experiment), DP = difference in blood content in the stomach between the beginning and the end of experiment, Bi = blood content in the stomach at the beginning of the experiment, F = weight of blood meal ingested (sum of intakes), and Be = blood contained in the stomach at the end of the experiment. These experiments were replicated for 20 5th instar nymphs and 15 females per food source.

Estimation of reproductive parameters

For these estimations, couples were formed and assigned randomly to one of the following two groups: Group 1: couples of adults fed regularly (every 15 days) on guinea pigs. Group 2: couples of adults fed regularly (every 15 days) on pigeons. Fourteen couples for group 1 and 15 for group 2 were followed until death. Couples were held in cylindrical glass vials. The females were weighed on the day of imaginal molt and before and after feeding to determine the amount of blood ingested at the adult stage and the mean blood ingested per feeding event. To make these data comparable with those obtained for other triatominae species, we weighed the bugs immediately after a blood meal and did not take into account the large diuresis that usually occurs after a blood meal (Catalá et al. 1992, Crocco and Catalá 1997, Guarneri et al. 2000, Sant'Anna et al. 2001, Nattero et al. 2011).

Twice a week we recorded the following variables from all of the 29 couples: number of eggs laid, number of eggs hatched, and number of spermatophores. Moreover, we recorded the days between the first feeding event and the onset of mating and oviposition, as well as the life span at the adult stage for each female. These parameters allowed us to calculate the blood to egg ratio (mg blood/egg) and the E value. The E values were calculated from Chiang and Chiang (1995), where E= total number of eggs/initial female weight × amount of blood ingested × 1,000.

Data analysis

We tested the assumptions of normality for all traits included in analysis using the Shapiro–Wilks test. We performed one-way ANOVA to determine whether the two estimates used for the food resource use, reproductive parameters and life span varied between blood meal sources (guinea pig and pigeon). Linear regressions were used to analyze the relationship between the amount of blood ingested and the number of matings and of eggs laid for the two blood meal sources and also to evaluate the relationship between copulation and oviposition onset.

RESULTS

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

For both 5th instar nymphs and females, the milligrams of blood consumed per day (CI) were significantly higher when bugs were fed on pigeons than on guinea pigs (Table 1). The quality of blood ingested did not affect ECB either for 5th instar nymphs or for females (Table 1).

Table 1.  Blood consumption index (CI) and efficiency of conversion of ingested blood (ECB) for Triatoma patagonica fed on blood of guinea pig and pigeon. Estimates were compared between meal sources with an ANOVA.
 5th instar nymphsFemales
 Blood meal sourceBlood meal source
 Guinea pig ×± SDPigeon ×± SDANOVA between meal sourcesGuinea pig ×± SDPigeon ×± SDANOVA between meal sources
CI (mg/day)5.08 ± 3.88 N= 209.02 ± 4.12 N= 20 F 1,37= 1.13; p= 0.0044.89 ± 2.27 N= 157.37 ± 1.96 N= 15 F 1,29= 1.34; p= 0.003
ECB (%)8.92 ± 25.30 N= 209.24 ± 23.32 N= 20 F 1,37= 0.00; p= 0.96627.28 ± 20.84 N= 1520.46 ± 24.61 N= 15 F 1,29= 1.39; p= 0.429

During adult life, females that were fed on pigeons ingested significantly more blood than when fed on guinea pigs (total blood ingested: 399.80 ± 169.29 mg and 234.43 ± 135.15; F= 8.37; df= 1, 28; p<0.01 for pigeons and guinea pigs, respectively). In addition, the effective number of feeding events showed significant differences (number of effective feedings: 3.64 ± 0.42 and 5.93 ± 0.41; F= 15.05; df= 1, 28; p< 0.001 for guinea pigs and pigeons, respectively).

Females fed on guinea pigs showed a significantly higher number of matings than those fed on pigeons. However, these differences did not translate into a higher fecundity or fertility, since the number of eggs laid and hatched did not show significant differences between food sources (Table 2). The onset of copulation and oviposition did not show significant differences between blood meal sources (Table 2). The amount of blood needed by a female fed on pigeon blood to produce an egg was significantly higher than for those females fed on guinea pig blood (Table 2). Moreover, the E value was significantly higher for females fed on guinea pig than for those fed on pigeon, whereas the latter had a longer life span than the former (Table 2).

Table 2.  Reproductive parameters and life span for couples of Triatoma patagonica fed on guinea pig and pigeon blood. Variables were compared between meal sources with an ANOVA. Days before onset of copulation and oviposition were calculated from the first feeding event in the adult stage.
VariablesBlood meal sourcesANOVA between blood meal sources
 Guinea pig x ± SD (N=14)Pigeon x ± SD (N= 5)
Onset of copulation (days)7.85 ± 5.165.67 ± 2.50 F 1,28= 2.17; p= 0.153
Number of matings6.00 ± 0.384.33 ± 0.37 F 1,28= 9.82; p= 0.004
Onset of oviposition (days)18.79 ± 15.6016.13 ± 13.05 F 1,28= 1.51; p= 0.230
Number of eggs laid52.65 ± 5.2644.15 ± 5.08 F 1,28= 1.40; p= 0.248
Proportion of eggs hatched0.75 ± 0.030.76 ± 0.03 F 1,28= 0.06; p= 0.802
Blood to egg ratio (mg blood/egg)4.49 ± 0.538.90 ± 0.99 F 1,28= 35.12; p= 0.000
E value1.61 ± 0.520.69 ± 0.16 F 1,28= 40.46; p= 0.000
Life span (days)63.00 ± 8.81104.00 ± 8.51 F 1,28= 11.19; p= 0.002

The number of eggs laid increased linearly and significantly with the amount of blood ingested for both sources (Figures 1A, 1B). A single copulation was enough to produce fertile eggs for both feeding sources. The number of matings did not show a significant linear relationship with the amount of blood ingested for both feeding sources (y= 6.23 + 0.99x, R2= 0.01, p= 0.77; y= 2.93 + 3.50x, R2= 0.23, p= 0.08, of guinea pig and pigeon blood, respectively). When the onset of copulation was regressed with the onset of oviposition, there was a positive and significant relationship for both meal sources (Figure 2).

image

Figure 1. Relationship between the amount of blood ingested and the number of eggs laid by Triatoma patagonica fed from two sources: (A) guinea pig. (B) pigeon.

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image

Figure 2. Relationship between the onset of copulation and onset of oviposition for Triatoma patagonica fed from two sources: (A) guinea pig. (B) pigeon.

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DISCUSSION

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

Our results agree with previous studies in which different triatomine species ingested larger amounts of blood when fed on birds rather than on mammals (Guarneri et al. 2000, Martínez-Ibarra et al. 2003). Intrinsic traits of bird and mammal triatomine hosts may explain these differences, such as the diameter or size of the erythrocytes and the hematocrit (Lehane 1991). Our results showed that for T. patagonica, females fed on pigeons had a greater number of effective feedings and larger blood meals ingested than those fed on guinea pigs. These results agree with records reported for T. sordida, which ingest higher amounts of blood when fed on pigeons than on guinea pigs (Crocco and Catalá 1997). This trend does not appear to be the same for all species, as T. infestans nymphs ingest higher amounts of blood when fed on guinea pigs than on pigeons (unpublished data).

The comparison of the CI between food sources showed that energetic requirements were significantly higher when both 5th instar nymphs and females fed on pigeon. Bird blood contains higher DNA concentration than mammal blood. The catabolism of nucleic acid and the resulting excretion of uric acid probably require an increase in energy consumption (Lehane 1991). The CI obtained for T. patagonica 5th instar nymphs was higher than that obtained for females (9.02 and 7.37 for 5th instar nymphs and females fed on pigeon blood, respectively) but lower than those obtained for T. infestans fed on pigeon blood (10.6 and 25.8 for 5th instar nymphs and females, respectively) (Catalá et al. 1992). On the other hand, the ECB was not influenced by the quality of blood ingested. The comparison of our results with those reported for T. infestans fed on pigeons shows that the ECB was similar for 5th instar nymphs of both species (9.02 and 10.6% for T. patagonica and for T. infestans, respectively) (Catalá et al. 1992). For females, as for nymphs, the efficiency of conversion of food into body substance did not differ among food sources. In females of T. patagonica, 20.46% of pigeon blood consumed became body substance. This value is similar to that recorded for females of T. infestans fed on pigeons (23.96%) (Montenegro and Pasina 1984), suggesting that both species would be equally efficient in converting blood into body substance. These results would indicate that although 5th instar nymphs and females met high energetic requirements with pigeon blood, the efficiency to transform the blood into body substance was not influenced by the quality of blood ingested. To our knowledge, this is the first time that these parameters are compared between blood meal sources for a triatomine species and further experiments with other species should be conducted to better understand this result of food resource use in these blood-sucking insects.

Regarding reproduction variables, fecundity expressed as total numbers of eggs did not differ between food sources, with an average of 48 eggs per female. This value is similar to that recorded in virgin females by Carrizo2 and intermediate to that recorded by Rodríguez1 for females fed every 21 days (20.5 eggs) and every seven days (72.1 eggs). Fecundity, as found in this work and reported by Carrizo2 and Rodríguez1 for T. patagonica, and for other species by Guarneri et al. (2000) and Nattero et al. (2011), among others, is related to the total intake during adult life. However, Carrizo2 and Rodríguez1 indicated that the first cycle of eggs laid is not dependent on blood intake in adult life; instead, given the autogenic nature of the species, the first egg cycle depends on the reserves that the females bring from 5th instar nymphs. Moreover, the onset of oviposition seems to be influenced by the onset of copulation. The onset of oviposition was found to be influenced by mating in T. patagonica (Lobbia3, Rodríguez et al. 2009) and in T. infestans (Asin and Crocco de Ayerbe 1989). Virgin females of this species, which were also fed on pigeon every 15 days, began oviposition at 38.2 ± 14.4 days, showing a delay with respect to the onset of oviposition recorded in the present study (16.13 ± 13.05 days for females fed on pigeon) (Carrizo2). Hence, in T. patagonica, as in other triatomine species, the stimulating effect of copulation on the muscles of the ovary and oviduct makes the fertilized females lay their eggs as fast as they are produced, whereas virgin females retain unfertile eggs in the ovary (Davey 2007).

The blood to egg ratio was high for those females fed on pigeon, which indicates that females feeding on this host need more blood to produce an egg than when fed on guinea pig. This high ratio reflects a low efficiency of conversion of blood to eggs. These results are consistent with those reported for other triatomine (Diotaiuti and Dias 1987, Gomes et al. 1990, Braga et al. 1999, Guarneri et al. 2000, Nattero et al. 2011), suggesting that mammal blood has a higher nutritional quality than bird blood and, as described above, digestion of pigeon blood requires an increased energy expenditure that may also influence reproductive parameters. The E value offers a measure of the individual fecundity in relation to the amount of blood ingested and of the blood remaining in the stomach from a 5th instar nymph (Chiang and Chiang 1995). According to this parameter, for T. patagonica, females fed on guinea pig laid 1.61 eggs/mg of blood, whereas those fed on pigeons laid 0.61 eggs/mg of blood. The E value obtained for pigeon was lower than that obtained by Rodríguez1 for T. patagonica (1.92 ± 2.89 eggs/mg of blood). The E value obtained in this work for pigeon was more similar to that obtained for the domiciliary species T. infestans and T. brasiliensis, of 0.54 to 0.94, respectively (Guarneri et al. 2000). For peridomiciliary species like T. pseudomaculata and T. sordida, these values are 2.10 to 2.43, respectively (Guarneri et al. 2000). The high amount of blood ingested and CI found for those females fed on pigeon does not translate into a high number of eggs laid and/or hatched. For other triatomine species, such as T. brasiliensis and T. sordida, a high number of eggs per female was observed in females fed on mammals (Guarneri et al. 2000, Daflon-Texeira et al. 2009), whereas for T. infestans, different results have been reported. Indeed, while Guarneri et al. (2000) did not find differences in the number of eggs laid between females fed on pigeon blood and those fed on mice blood, Nattero et al. (2011) did find significant differences between females fed on pigeon blood and those fed on guinea pig blood. For T. pseudomaculata, Guarneri et al. (2000) found no difference in the number of eggs laid between females fed on those food sources. These results suggest that triatomine species do not show a trend to lay a high number of eggs when fed on mammalian blood. The number of eggs hatched is similar, although lower, than that reported for other peridomestic species fed on birds, such as T. sordida (Oscherov et al. 1998), T. guasayana (Ghilini 1982), and T. platensis (Bar et al. 1986), in which fertility percentage higher than 80% was recorded. Results found in this work suggest that a single copulation would be enough for fertile oviposition. This fact is important from an epidemiological point of view, because those females that have mated once may lay fertile eggs, thereby increasing the chances of forming new colonies. For other triatomine species, it has been stated that only one mating is enough for a female to maintain fertile eggs for her entire life span (Lima et al. 1987, Pires et al. 2004). In T. brasiliensis, T. infestans, and Rhodnius prolixus females need more than one copulation to ensure fertile ovipositions (Stoka et al. 1987, Daflon-Texeira et al. 2009, Pontes and Lorenzo 2011) Moreover, in T. infestans and Rhodnius prolixus, males aggregated around a mating couple and several copulations occurred (Pontes and Lorenzo 2011).

The peridomestic environment was defined as unstable compared to the domestic one based on environmental characteristics, such as marked fluctuations in temperature and humidity and the scarce or unstable availability of food resources (Dujardin et al. 1997, Dujardin et al. 1999, Schofield 1999). Thus, females living in such unstable environments would invest more energy into reproduction. On the other hand, and due to characteristics of this environment, bugs can circulate among different peridomestic structures, taking blood both from bird and mammal domestic hosts. Triatoma patagonica is mainly adapted to peridomestic structures. The results found in this study show that the higher amount of blood ingested and consumed by T. patagonica fed on pigeons did not translate into a higher fecundity or fertility. The lower amount of guinea pig blood ingested would be offset by its high nutritional quality. Under natural conditions for T. patagonica it would be a selective advantage to prevent restrictions on its reproductive success by using available hosts, either mammals or birds.

Acknowledgments

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

We are grateful to G. Leonhard and R. Stariolo (Centro de Referencia de Vectores, Córdoba, Argentina) for supplying the insects necessary for the development of this study. Patricia Lobbia and Sebastián Ravinale helped us in the laboratory work. JN and CSR are fellow researchers and scholarship holders at CONICET, respectively. This study was funded by the Secretaría de Ciencia y Técnica Universidad Nacional de Córdoba.

Footnotes
  • 1

    Rodríguez, C.S. 2011. Características de Triatoma patagonica (Hemiptera: Reduviidae) relacionadas con la capacidad de colonizar el hábitat intradomiciliar. PhD Tesis. Universidad Nacional de Córdoba, Córdoba.

  • 2

    Carrizo, S.A. 2003. Efecto del ayuno sobre la capacidad reproductiva de Triatoma patagonica (Del Ponte, 1929) (Hemiptera, Reduviidae). Tesis de Grado, Universidad Nacional de Córdoba, Córdoba.

  • 3

    Lobbia, P.A. 2009. Patrón de desarrollo ovárico en hembras de Triatoma patagonica Del Ponte, 1929 (Hemiptera: Reduviidae). Tesis de Grado, Universidad Nacional de Córdoba, Córdoba.

REFERENCES CITED

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  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED
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