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Temperature during larval development and adult maintenance influences the survival of Anopheles gambiae s.s. Céline Christiansen-Jucht1*, Paul E Parham3,5, Adam Saddler2, Jacob C Koella2,4 and María-Gloria Basáñez1

Abstract Background: Malaria transmission depends on vector life-history parameters and population dynamics, and particularly on the survival of adult Anopheles mosquitoes. These dynamics are sensitive to climatic and environmental factors, and temperature is a particularly important driver. Data currently exist on the influence of constant and fluctuating adult environmental temperature on adult Anopheles gambiae s.s. survival and on the effect of larval environmental temperature on larval survival, but none on how larval temperature affects adult life-history parameters. Methods: Mosquito larvae and pupae were reared individually at different temperatures (23 ± 1°C, 27 ± 1°C, 31 ± 1°C, and 35 ± 1°C), 75 ± 5% relative humidity. Upon emergence into imagoes, individual adult females were either left at their larval temperature or placed at a different temperature within the range above. Survival was monitored every 24 hours and data were analysed using non-parametric and parametric methods. The Gompertz distribution fitted the survivorship data better than the gamma, Weibull, and exponential distributions overall and was adopted to describe mosquito mortality rates. Results: Increasing environmental temperature during the larval stages decreased larval survival (p < 0.001). Increases of 4°C (from 23°C to 27°C, 27°C to 31°C, and 31°C to 35°C), 8°C (27°C to 35°C) and 12°C (23°C to 35°C) statistically significantly increased larval mortality (p < 0.001). Higher environmental temperature during the adult stages significantly lowered adult survival overall (p < 0.001), with increases of 4°C and 8°C significantly influencing survival (p < 0.001). Increasing the larval environment temperature also significantly increased adult mortality overall (p < 0.001): a 4°C increase (23°C to 27°C) did not significantly affect adult survival (p > 0.05), but an 8°C increase did (p < 0.05). The effect of a 4°C increase in larval temperature from 27°C to 31°C depended on the adult environmental temperature. The data also suggest that differences between the temperatures of the larval and adult environments affects adult mosquito survival. Conclusions: Environmental temperature affects Anopheles survival directly during the juvenile and adult stages, and indirectly, since temperature during larval development significantly influences adult survival. These results will help to parameterise more reliable mathematical models investigating the potential impact of temperature and global warming on malaria transmission. Keywords: Anopheles gambiae sensu stricto, Environmental temperature, Larval survival, Mosquito survival, Climate change

* Correspondence: [email protected] 1 Department of Infectious Disease Epidemiology, School of Public Health, Faculty of Medicine (St Mary’s campus), Imperial College London, Norfolk Place, London W2 1PG, UK Full list of author information is available at the end of the article © 2014 Christiansen-Jucht et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Christiansen-Jucht et al. Parasites & Vectors 2014, 7:489 http://www.parasitesandvectors.com/content/7/1/489

Background Although historical data and theoretical models suggest that the distribution of malaria is much more sensitive to the scale-up of control measures than to climate change, it appears evident that climate change will affect the distribution and transmission of mosquito-borne diseases such as malaria [1] and thereby influence the extent to which the disease can be controlled. However, we currently have a limited understanding of how climatic factors affect the entomological parameters determining transmission. The most obvious question is how increasing temperatures associated with climate change will affect mosquito longevity and the duration of the parasite’s development within the mosquito, two of the most influential parameters underlying the transmission of mosquito-borne diseases. However, temperature also shapes mosquito life-history traits that are associated with vector-competence and determines mosquito population density: a warmer environment leads to faster development and smaller adults. Mosquito size can influence epidemiologically relevant traits such as longevity, length of the gonotrophic cycle, immunocompetence, size of the bloodmeal (and probability of infection), biting rate, and intensity of infection. These traits in turn can affect mosquito survi