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Revista da Sociedade Brasileira de Medicina Tropical

Print version ISSN 0037-8682

Rev. Soc. Bras. Med. Trop. vol.47 no.4 Uberaba July/Aug. 2014

http://dx.doi.org/10.1590/0037-8682-0111-2014 

Major Articles

Effect of feeding frequency on the reproductive efficiency of two species of Triatoma with different epidemiological importance

Claudia Rodríguez[1] 

Patricia Lobbia[2] 

Julieta Nattero[1] 

Silvia Catalá[3] 

Liliana Crocco[1] 

[1]Cátedra de Introducción a la Biología, Instituto de Investigaciones Biológicas y Tecnológicas, Facultad de Ciencias Exactas, Físicas y Naturales, Universidad Nacional de Córdoba, Córdoba, Argentina

[2]Centro de Referencias de Vectores, Pabellón Rawson, Hospital Colonia de Santa María de Punilla, Santa María de Punilla, Córdoba, Argentina

[3], Anillaco, La Rioja, Argentina

ABSTRACT

Introduction

In Triatominae, reproductive efficiency is an important factor influencing population dynamics, and a useful parameter in measuring a species' epidemiological significance as a vector of Trypanosoma cruzi (Chagas, 1909). The reproductive efficiency of triatomines is affected by food availability; hence, we measured and compared the effects of feeding frequency on the reproductive parameters of Triatoma patagonica (Del Ponte, 1929) and Triatoma infestans (Klug, 1934), and the effects of starvation on T. patagonica.

Methods

Couples from both species were fed weekly, or every 3 weeks; in addition, females in couples of T. patagonica were not fed. Each couple was observed weekly and reproductive efficiency was assessed on the following parameters: fecundity (eggs/female), fertility (eggs hatched/eggs laid), initiation and end of oviposition, initiation of mating, number of matings/week, and number of reproductive weeks. Relative meal size index (RMS), blood consumption index (CI), and E values (eggs/mg blood) were also calculated.

Results

Changes in feeding frequency affected the reproductive parameters of T. patagonica only, with a decrease in fecundity and number of reproductive weeks for those fed every 3 weeks, or not fed. The reproductive period, RMS index, and CI were lower for T. patagonica than T. infestans. However, despite the lower fecundity of T. patagonica, this species required less blood to produce eggs, with an E values of 2 compared to 2.94 for T. infestans.

Conclusions

Our results suggest that the differences in fecundity observed between species reflect the availability of food in their natural ecotopes.

Key words: Blood-sucking insect; Chagas disease; Fecundity; Fertility; Triatominae

INTRODUCTION

In Latin America, triatomines (Hemiptera: Reduviidae) are recognized vectors of Trypanosoma cruzi, the etiological agent of Chagas disease. Although these hematophagous insects are of wild origin, several species show varying levels of ecological adaptation to human habitats1,2, and this trait is relevant in characterizing the epidemiological importance of these species1.

Of the 140 species in this subfamily3, 18 occupy wild habitats in Argentina, in addition to intradomicile and peridomicile environments4. Triatoma infestans is one species that has successfully adapted to human habitats. This primary vector has a wide distribution in southern South America, and is the most epidemiologically important species in Argentina, colonizing intradomicile and peridomicile environments, where it is associated with birds, and occasionally mammals4. In addition, Triatoma infestans has been shown to have a significant level of natural infection with T. cruzi1,5,6.

Triatoma patagonica occupies wild and peridomestic habitats, and has only been reported in Argentina to date, with its southernmost distribution limited to the Chubut province of Patagonia7. This secondary vector8 has been shown to establish significant colonies in peridomestic ecotopes9, where it feeds on both birds and mammals7, and a few instances of intradomicile colonization have been recorded10,11. Triatoma infestans and T. patagonica can colonize different peridomestic structures, feeding on both birds and mammals; in rural areas of Argentina, chicken coops are the most common of such structures12,13, and thus, in these habitats T. infestans feeds predominantly on chickens, as opposed to dogs or goats12,14.

The reproductive efficiency of a species is strongly associated with its potential to colonize or recolonize a habitat; thus, information on its effects on population dynamics may help to determine the epidemiological significance of different triatomine species15,16. Reproductive efficiency, as determined by parameters related to fecundity and fertility15,17, may vary between species of triatomines; however, within species, this variation is significantly affected by factors such as environment (temperature), physiology (insect age, and gonadotrophic cycle status) and food (volume, quality, and availability)18. Food availability in the wild varies and insects may feed daily or undergo prolonged fasting, with each species having a critical feeding frequency at which reproductive parameters begin to be affected19.

In adult female triatomines, blood meals are essential for egg production, as they stimulate endocrine regulation of ovarian development20. However, females that have high nutritional reserves from the fifth-instar nymph stage can undergo the first cycle of egg production without feeding20. This phenomenon, known as autogeny, has been described for several triatomine species2123, including T. infestans23 and T. patagonica24. However, reproductive parameters under fasting conditions for the latter have yet to be fully described.

Abalos25 has questioned whether T. patagonica could replace T. infestans as a permanent host of T. cruzi in intradomiciliary environments in southern Argentina. Considering that these species, which have a different epidemiological importance, coexist in peridomiciliary habitats, the objective of this work was to compare the effects of different food supply frequencies and starvation conditions on their reproductive parameters.

METHODS

Triatoma patagonica and Triatoma infestans were supplied by the Coordinación Nacional de Control de Vectores (Córdoba province, Argentina). These insects were originally obtained from chicken coops in the San Luis and La Rioja provinces (Argentina). First-generation insects were reared from eggs in our laboratory and maintained under controlled temperature (26 ± 1°C) and relative humidity (60 ± 10%), and a photoperiod of 12:12h (light: dark). Groups of 15 insects were kept in cylindrical (500cm3) glass bottles covered with nylon mesh and containing vertically folded paper to allow insects' access to food and to avoid excess humidity. Triatomines were allowed to feed for 30 min on an immobilized pigeon (Columba livia Gamelin) placed on a plastic box. First-instar nymphs of each species were divided into 2 groups and fed either weekly, or every 3 weeks, from the nymphal to the adult stage.

Once triatomines had reached the adult stage (between August and September), couples from each group, for both species, were placed in separate glass bottles until both insects died. The 4 groups were defined as follows: G1: 13 couples of T. patagonica fed once a week; G2: 13 couples of T. patagonica fed every 3 weeks; G3: 10 couples of T. infestans fed once a week; and G4: 13 couples of T. infestans fed every 3 weeks.

In addition, an autogenic group comprised 13 couples of T. patagonica, which were fed every 2 weeks throughout the nymphal stage, and then females were not fed, and males were fed once a week, for the adult stage.

Reproductive parameters

Couples were observed weekly until females died, and the following data were recorded: initiation and end of oviposition; initiation of mating; matings per week (determined by observation of spermatophores); reproductive weeks, fecundity (number of eggs laid/female); age-specific fecundity (mx = mean eggs/female/week); and fertility (number of eggs hatched/number of eggs laid), calculated as: (number of eggs hatched/total eggs) × 100. The length of the adult stage (days) for females was also recorded. Eggs were stored in Eppendorf tubes until nymphs hatched.

Relationships between feeding frequency and reproductive parameters

Females were weighed on the day of imaginal molt, and before and after each feeding event, to calculate the amount of blood consumed. The relative meal size index (RMS = meal size/insect weight before feeding) was calculated to allow comparison between species26.

The blood consumption index (CI) was calculated for each group as per Catalá et al.27 using the following formula: CI = [(Bi + F) − Be]/T, where Bi is blood in the stomach at moulting; F is the weight of ingested food (sum of intakes); Be is blood in the stomach after the last feeding event; and T is the duration of the adult stage (days). Blood contained in the stomach (BCS) was calculated using the following equations: BCS = −69.76 + 0.54x and BCS = −14.07 + 0.32x, as described by Catalá de Montenegro28 for T. infestans and Nattero et al.29 for T. patagonica, respectively. E values were calculated as follows: [total number of eggs/(initial female weight × amount of blood ingested)] × 1,00030.

All weight measurements were performed using a Mettler Toledo precision balance (PG203-S) to a level of 0.001g.

Data analysis

Means and standard deviations were calculated for each variable. If data for variables did not show normal distribution or homogeneity of variance, as analyzed by the Kolmogorov-Smirnov and Levene's tests respectively, groups were compared using a non-parametric Mann-Whitney test (statistical index U) or Kruskal-Wallis one-way analysis of variance (statistical index U). Spearman's correlation coefficient (rs) was used to evaluate correlations between reproductive parameters and feeding behavior for each species. Percentages were compared using Fisher's test. A p-value <0.05 was considered statistically significant.

RESULTS

Only couples in which females laid eggs were considered in the analysis of reproductive efficiency and feeding behavior. All T. infestans females (n = 23/23, groups G3 and G4) and 65.38% (n = 17/26, groups G1 and G2) of T. patagonica females laid eggs at least once, and data from these groups was further examined (Table 1).

TABLE 1-  Reproductive parameters for Triatoma patagonica and Triatoma infestans females with different feeding regimens (G1 and G3: fed weekly; G2 and G4: fed every 3 weeks). 

Triatoma patagonica Triatoma infestans
G1 n = 9 G2 n = 8 Mann-Whitney test U (p-value) G3 n = 11 G4 n = 12 Mann-Whitney test U (p-value)
Initiation of oviposition (days) 31.33 ± 17.65 23.25 ± 6.75 33.5 (0.06) 6.22 ± 7.08 4.80 ± 10.04 26.5 (0.36)
Fecundity (eggs/female) 72.11 ± 66.0 20.50 ± 14.48 15.0 (0.04) 183.3 ± 118.33 132.61 ± 113.21 41.1 (0.14)
Reproductive weeks 10.0 ± 7.14 4.12 ± 2.85 13.5 (0.06) 26.24 ± 9.22 33.61 ± 18.24 49.5 (0.33)
Initiation of mating (days) 31.33 ± 17.65 23.25 ± 6.75 43.0 (0.87) 6.22 ± 7.08 4.80 ± 10.04 32.0 (0.10)
Number of matings 10.0 ± 7.14 4.12 ± 2.85 24.5 (0.26) 33.61 ± 18.24 26.4 ± 9.22 56.0 (0.79)
Fertility (%) 72.1 ± 66.0 20.5 ± 14.5 18.0 (0.24) 56.3 ± 22.3 66.7 ± 34.9 44.5 (0.30)

: mean ± standard deviation; n: number of insects; U: statistical index of Mann-Whitney test.

Female longevity was similar within each species for both feeding regimens. However, T. patagonica females had a significantly shorter lifespan than T. infestans females with a mean age of 77.92 ± 64.81 days compared to 316.60 ± 95.58 days (H = 33.91, p < 0.001).

Reproductive parameters

Fecundity was significantly higher in T. patagonica females fed once a week (G1) than those fed every 3 weeks (G2; p < 0.05; Table 1); however, there were no significant differences between feeding frequency for other reproductive parameters measured for this species (Table 1). For T. infestans there were no significant differences between groups for any of the reproductive parameters measured (Table 1).

Oviposition (H = 16.62, d.f. = 3, p = 0.0008) and mating (H = 16.17, d.f. = 3, p = 0.01) began earlier in T. patagonica than T. infestans; however, fecundity and reproductive weeks were higher for T. infestans (H = 17.62, d.f. = 3, p = 0.005 and H = 25.58, d.f. = 3, p < 0.0001 for fecundity and reproductive weeks respectively).

Of all couples observed, 88.2% (n = 15/17) of T. patagonica and 78.3% (n = 18/23) of T. infestans mated at least once, with no difference between species (p = 0.209, Fisher exact test). The mean mating number was significantly higher for T. infestans than T. patagonica (H = 7.94, d.f. = 3, p = 0.04), and the fertility rate was below 62.0%, with no differences between species (U = 132.00, p = 0.307; Table 1).

In T. patagonica reproductive activity began at week 2 and week 3 for G1 and G2 respectively, with the maximum reproductive effort (mx) recorded at week 6 for G1 and week 4 for G2 (mean mx 9.24 ± 6.18 and 5.90 ± 4.52 eggs/female/week for G1 and G2 respectively) with no significant difference between groups (U = 24.00, p = 0.24). From week 7 for G1 and week 13 for G2, mx values began to decrease until females stopped laying eggs; however, there were a number of additional reproductive peaks for G2 (Figure 1A). In T. infestans, reproductive activity began at week 2 for both groups, and mean mx values did not differ significantly between groups (U = 36.00, p = 0.07) (mean mx 7.43 ± 4.51 and 4.56 ± 3.91 eggs/female/week for G3 and G4 respectively). The maximum reproductive effort for this species was recorded at the end of the reproductive period, at week 41 for G3 (26 eggs/female) and at week 65 for G4 (32 eggs/female; Figure 1B).

FIGURE 1-  Age-specific fecundity curves (mx) for (A) Triatoma patagonica and (B) Triatoma infestans females with different feeding regimens. Dotted lines: groups fed weekly (G1 and G3); Continuous lines: groups fed every 3 weeks (G2 and G4). 

For both species, the number of matings positively correlated with fecundity (rs = 0.64, p = 0.004 and rs = 0.56, p = 0.006, for T. infestans and T. patagonica respectively). For T. infestans females, there was also a correlation between initiation of oviposition and mating (rs = 0.53, p = 0.013).

Initiation of oviposition (20.23 ± 8.2 days), first mating (14.33 ± 3.70 days), and fertility (53.75 ± 40.85%) for the autogenic group of T. patagonica (autogenic group) showed similar values to those for G1 and G2 (H = 3.78, p = 0.15; H = 3.52, p = 0.17 and H = 5.90, p = 0.052 respectively). However, the number of reproductive weeks (2.92 ± 1.75) of the autogenic group was lower than that for other groups (H = 9.07, p = 0.01), and fecundity (16.38 ± 7.81 eggs per female) was significantly lower than G1 and similar to G2 (H = 9.57, p = 0.008).

Relationships between feeding frequency and reproductive parameters

Only G1 and G2 groups were analyzed in terms of relationships between feeding frequency and reproductive parameters.

The weight at moulting of the T. patagonica G1 group was higher than that of G2; however, there were no significant differences between the G3 and G4 groups of T. infestans. For both species, the volume of blood ingested in the adult stage was similar for females fed weekly or every 3 weeks (Table 2). T. infestans females had a higher RMS index and blood CI than T. patagonica, when fed weekly (U = 10.00, p = 0.007 and U = 5.00, p = 0.002 for RMS and CI, respectively) and every 3 weeks (U = 0.00, p = 0.006 and U = 11.00, p = 0.003 for RMS and CI, respectively; Table 2).

TABLE 2-  Amount of blood ingested, relative meal size index, blood consumption index and E values for Triatoma patagonica and Triatoma infestans (G1 and G3: fed weekly; G2 and G4: fed every 3 weeks). 

Triatoma patagonica Triatoma infestans
G1 n = 7 G2 n = 4 Mann-Whitney test U (p-value) G3 n = 10 G4 n = 13 Mann-Whitney test U (p-value)
Weight at molting (mg) 186.1 ± 30.6 146.5 ± 45.2 33.5 (0.009) 247.5 ± 56.4 218.2 ± 60.2 45.0 (0.21)
Blood ingested (mg) 439.5 ± 350.5 116.0 ± 114.4 16.0 (0.09) 2071.7 ± 798.5 2192.6 ± 1221.0 64.0 (0.95)
RMS 3.95 ± 3.84 0.69 ± 0.71 8.0 (0.04) 10.76 ± 6.49 8.67 ± 4.42 51.0 (0.38)
CI (mg/day) 3.35 ± 1.47 2.37 ± 2.07 18.0 (0.14) 7.08 ± 2.14 6.13 ± 2.42 39.0 (0.19)
E value (eggs/mg blood) 1.58 ± 1.25 2.40 ± 4.49 9.0 (0.16) 0.50 ± 0.39 0.21 ± 0.09 24.0 (0.01)

: mean ± standard deviation; n: number of insects; U: statistical index of Mann-Whitney test; RMS: relative meal size index; CI: consumption index.

For T. patagonica, oviposition began before the first feeding event for 33.3% and 62.5% of females for G1 and G2 respectively; however, for T. infestans, no females laid eggs without being fed at least once.

For T. patagonica females, there were no statistically significant differences for E values in relation to feeding frequency, and standard deviations were high. However, these E values were significantly higher than those recorded for both groups of T. infestans females (H = 20.47, d.f. = 3, p = 0.0001; Table 2).

For both species, the volume of blood ingested during the adult stage correlated positively with fertility (rs = 0.62, p = 0.030 for T. patagonica and rs = 0.60, p = 0.05 for T. infestans) and reproductive weeks (rs = 0.85, p = 0.0003 for T. patagonica and rs = 0.54, p = 0.05 for T. infestans).

DISCUSSION

Feeding has a direct effect on the reproductive efficiency of triatomines. Variations in reproductive parameters within species relate to food availability, quality, and nutritional status18, whereas differences between species may be due to the relationship between reproductive behavior and the insects' natural habitat15. Consensus has not yet been reached in terms of the quality of ingested blood, with some species showing greater reproductive efficiency when fed on mammals or birds15,17,29, but other species not15; variability has even been shown between different studies of the same species15,29. For this reason, our results are discussed in the context of other studies using the same food source. The reproductive efficiency of T. infestans females does not appear to be affected by feeding frequency, as there were no differences between groups for any reproductive parameters. However, the reproductive efficiency of the secondary vector T. patagonica appears to be sensitive to feeding frequency, as fecundity, reproductive weeks, and blood consumption, were lower in females fed every 3 weeks than those was fed weekly. Similarly, Zeledón et al.21 and Cabello et al.19 reported an increase in fecundity with increased feeding frequency for Triatoma dimidiata and Rhodnius neivai.

On the other hand, the fact that T. patagonica that were starved had similar fecundity and reproductive week values to those of females fed every 3 weeks suggests that this is close to the critical fasting limit for this species in terms of reproductive parameters.

Females of T. patagonica began to lay eggs earlier than T. infestans. This may be related to the stimulatory effects of mating on oviposition20, as females of this peridomiciliary species copulated earlier than those of the domiciliary species. In T. infestans31 and other domiciliary triatomine species like Panstrongylus megistus32 and Triatoma brasiliensis13, virgin females were found to begin laying eggs later than those that had copulated. Accordingly, Carrizo24 reported that virgin females of T. patagonica fed fortnightly began oviposition at 38.2 ± 14.4 days, later than that recorded here.

Fecundity and reproductive weeks were also different between species, with values for both higher in T. infestans than T. patagonica. However, the fecundity values under starvation for T. patagonica seen in this study were higher than those reported by Noriega20 for T. infestans under similar conditions. This may be an advantageous characteristic in T. patagonica, allowing it to lay many eggs prior to first feeding in a peridomicile habitat where food availability is variable. For both species, fertility rates were similar; however, they were lower than values previously recorded for these species7,26,33, as well as other peridomiciliary and domiciliary species7,34,35 fed on birds blood. This decrease might be due to excessive insect manipulation during the performance of experiments, and is in agreement with results reported by Tolesano et al.36 for T. infestans.

Reproductive efficiency in terms of fecundity was compared between species by calculating indices relating egg production to blood consumption. Although T. patagonica laid fewer eggs and had a lower RMS than T. infestans, they consumed a smaller volume of blood daily (CI) and were more efficient in converting blood into eggs (E values), producing approximately 2 eggs per mg blood ingested. To produce a similar number of eggs, T. infestans required approximately 4mg of blood when fed weekly. The E values obtained in this work are similar to those reported by Guarneri et al.15 for other domiciliary and peridomiciliary species. These authors indicated that differences in E values between species reflect the food availability of the insects' natural ecotopes.

In the natural environments of triatomine species, there are a number of interacting factors that cannot be reproduced in the laboratory, such as behavioral responses to the environment and to different food sources, and genetic variability of populations34,37. Hence, although it is difficult to extrapolate the data presented here directly to populations developing in natural environments, our results do indicate trends in the behavior of these species relative to these environments.

Our comparison of the reproductive efficiency of these two species with different epidemiological importance indicates that, unlike domiciliary species, peridomiciliary species such as T. patagonica allocate a greater percentage of ingested blood to reproduction than maintenance. This characteristic may be related to the environmental conditions under which this species develops. Peridomiciliary species live in unstable ecotopes, and form small scattered colonies with infrequent access to food sources, whereas domiciliary species live in more stable ecotopes in high densities and with frequent food access.

CONFLICT OF INTEREST

The authors declare that there is no conflict of interest.

FINANCIAL SUPPORT

This study was funded by the Secretaría de Ciencia y Técnica, Universidad Nacional de Córdoba (05/1554).

ACKNOWLEDGMENTS

We thank the Coordinación Nacional de Control de Vectores (Santa María de Punilla, Córdoba, Argentina) for providing specimens of T. patagonica and T. infestans; Walter Almirón, Gabriel Manrique, and Jorge Rabinovich for their contribution to the development of experiments; and Jorgelina Brasca for language editing.

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Received: May 15, 2014; Accepted: July 8, 2014

Address to: Dra Claudia S. Rodríguez. Cátedra Introducción a la Biología/Facultad de Ciencias Exactas, Físicas y Naturales/UNC. Av. Vélez Sarsfield 299, piso 5, X5000JJC Córdoba, Argentina. Phone: 54 351 433-2100 ext. 248. e-mail: claudiarodriguez@efn.uncor.edu

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