Thermal Ecology of a Malarial Parasite and its Insect Vector: Consequences for the Parasite's Transmission Success

Abstract

We examined the transmission biology of Plasmodium mexicanum, a parasite of the fence lizard Sceloporus occidentalis, and its vector, the sandfly Lutzomyia vexator. Female L. vexator produced a clutch of eggs after each blood meal taken from a lizard. Mortality was high after oviposition, so few sandflies were likely to take two blood meals and almost none took three. Therefore, to maximize its transmission success, the parasite must complete development in its insect host before the vector lays its eggs and takes another blood meal. Between 16°C and 32°C, temperature did not affect the longevity of female sandflies, but did affect the rate of parasite development in the insect, the rate of maturation of sandflies' eggs, and the probability of sandflies becoming infected. The above relationships with temperature were non-linear and differed in shape among the variables such that an increase in temperature between 22°C and 32°C benefited the parasite by shortening its development while not reducing the time until the sandfly's next blood meal. We measured the temperatures available to the vectors in nature (burrows of ground squirrels). Within this range, there was a window that allowed successful transmission of the parasite (based on laboratory studies). In a thermal gradient, unfed female sandflies selected mean temperatures approximately 4°C below the minimum required for transmission. After a blood meal from a non-infected lizard, the insect's mean preferred temperature increased 1.6°C, presumably to aid digestion, and if a blood meal was taken from an infected lizard mean preferred body temperature increased by 3.6°C. Compared with 10 other Plasmodium species, P. mexicanum has a very rapid rate of development in its vector. The results suggest P. mexicanum enhances its transmission success through a combination of rapid development in the insect host and manipulation of the vector's thermoregulatory behaviour.