A physiological time analysis of the duration of the gonotrophic cycle of Anopheles pseudopunctipennis and its implications for malaria transmission in Bolivia

Abstract

Background: The length of the gonotrophic cycle varies the vectorial capacity of a mosquito vector and therefore its exact estimation is important in epidemiological modelling. Because the gonotrophic cycle length depends on temperature, its estimation can be satisfactorily computed by means of physiological time analysis.

Methods: A model of physiological time was developed and calibrated for Anopheles pseudopunctipennis, one of the main malaria vectors in South America, using data from laboratory temperature controlled experiments. The model was validated under varying temperatures and could predict the time elapsed from blood engorgement to oviposition according to the temperature.

Results: In laboratory experiments, a batch of An. pseudopunctipennis fed at the same time may lay eggs during several consecutive nights (2-3 at high temperature and > 10 at low temperature). The model took into account such pattern and was used to predict the range of the gonotrophic cycle duration of An. pseudopunctipennis in four characteristic sites of Bolivia. It showed that the predicted cycle duration for An. pseudopunctipennis exhibited a seasonal pattern, with higher variances where climatic conditions were less stable. Predicted mean values of the (minimum) duration ranged from 3.3 days up to > 10 days, depending on the season and the geographical location. The analysis of ovaries development stages of field collected biting mosquitoes indicated that the phase 1 of Beklemishev might be of significant duration for An. pseudopunctipennis. The gonotrophic cycle length of An. pseudopunctipennis correlates with malaria transmission patterns observed in Bolivia which depend on locations and seasons.

Conclusion: A new presentation of cycle length results taking into account the number of ovipositing nights and the proportion of mosquitoes laying eggs is suggested. The present approach using physiological time analysis might serve as an outline to other similar studies and allows the inclusion of temperature effects on the gonotrophic cycle in transmission models. However, to better explore the effects of temperature on malaria transmission, the others parameters of the vectorial capacity should be included in the analysis and modelled accordingly.

Figure 1

A generalized insect developmental rate curve as a function of temperature: the Lactin et al. function [20]. Descriptive parameters are T_base, the base temperature below which development does not proceed, the maximum development rate r_max and its corresponding temperature T_upper, the width Δ of decline phase in developmental rate above optimum temperature and the thermal maximum T_m.

Figure 2

Relation between mean development rate (MDR) and its standard deviation (SD) at various constant temperatures. Each point is labelled by the temperature value (in °C) from the experimental chamber. The regression line is SD = -0.0017 + 0.1859 MDR, with R² = 0.91.

Figure 3

Egg laying patterns for An. pseudopunctipennis at various constant temperatures. The number of ovipositing nights is pictured by the observed "pulses" which have a pseudo Gaussian mode.

Figure 4

Physiological time model for egg maturation of An. Pseudopunctipennis. For cohort 5, 6 and beyond, there were not enough points to estimate the Lactin et al function parameters.

Figure 5

Model predictions of length of the gonotrophic cycle (Phase 2 of Beklemishev) for An. pseudopunctipennis in a field resting place. Temperature data permitting computations were collected from June 2002 to January 2004, with recording stops in September 2002 and February 2003. Cycle duration is in days.

Figure 6

Model predictions of length of the gonotrophic cycle (Phase 2 of Beklemishev) for An. pseudopunctipennis in four representative localities of Bolivia. a. Localities of Sucre, Aiquile and Mataral, from January 1998 to December 2000. b. Localities of Yacuiba and Mataral (as a baseline comparison), from January 1998 to December 2000. Cycle durations are in days.

Figure 7

Cox model representation of An. pseudopunctipennis mortalities at various constant temperatures. The model expresses the instantaneous risk of mortality according to the temperature.