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Do we need to think more about gonotrophic cycles in mosquitoes and the effect they might have on parasite transmission?

May 5, 2012 - 15:32 -- Derek Charlwood

There is apparently considerable discussion about early biting shifts in mosquitoes like An. arabiensis.  (Why this might be so I hope to describe below – but be warned in a recent submission a referee questioned the number of Charlwood references quoted – I had to reply well they are really the only ones I know, and no one reads them anymore so why not – a bit like insinuating an obscure word that no one has ever read before into a text! - so you might at least know what to expect if I write anymore of them. i.e. not really the most learned or up to date discussion – feel free to bring me up to speed on what is going on out there in what the Water Rat, in Wind in the Willows, described as the ‘wide world’ Cat Stevens is singing about it as I write from the hot seat in Pailin, where ACT resistance was first described, last stronghold of the Khmer Rouge!)

Anyway it seems to me that discussion concerning these shifts has been focussed on the threat of outdoor exposure in the early evening (exposure which, of course, may change with moon phase) and transmission at such times obviously needs to be addressed.  Little or no thought has, however, been given to the effect that such a shift in biting has on the overall gonotrophic cycle length.  Egg development in mosquitoes is known to depend on temperature.  Oviposition is a ‘Gated’ phenomenon.  Anophelines like Anopheles funestus oviposit just after sunset.  If their eggs are ready to be laid halfway through the night the mosquito (and by inference the parasite she may be harbouring) will not leave but will stay inside the house and so experience an additional 18hrs of indoor temperatures per gonotrophic cycle (almost a third longer).  Since survival is to be thought of as survival per gonotrophic cycle rather than in calendar days this may have a big impact on transmission (and post-prandial resting has little impact on mortality).  I am not sure how much information though is out there on egg development times in An. funestus  and An. gambiae at different temperatures.  Maybe there is a ‘best’ and worst time to be bitten (in the sense that by restricting the mosquito to a two day cycle, all fed females completing egg development shortly before dusk, the number of hazardous events the mosquito has to survive before becoming a living hypodermic is increased.  (The blocking of salivary glands effectively turns the mosquito into the extended phenotype of the parasite essentially decoupling the relationship between survival rate and vectorial capacity.  How many times have I seen whole families in isolated areas with low mosquito densities simultaneously ill with malaria in the Amazon or PNG?  The trend towards individual bedrooms in many parts of Africa, such as The Gambia, may unwittingly be a good way to reduce transmission, although I am not sure what the word is on attractiveness of four people in four houses or four people in a single house).   With the information on biting time and development rate at temperature X the number of degree days experienced by the parasite can be determined.  What then is left is the time spent finding an oviposition site, laying eggs and returning to feed (which is an outdoor temperature).  This is known to vary with moon phase (although other meteorological factors such as cloud cover may ameliorate these effects) and as Gillies showed for An. funestus at least with temperature.

This is found out by examination of the mosquitoes ovaries.  I was fortunate to have been taught the technique by the Maestro himself, my very good friend, Tony Wilkes.  Mosquitoes that return to feed shortly after oviposition have large ovariolar sacs – that recently held the egg - whereas those that delay have small ones.

Now one thing we found in Papua New Guinea with the mosquito Anopheles farauti was that when mosquito nets were introduced into a village being unable to feed as easily as they had before the mosquito population changed from one in which most mosquitoes had a two day cycle to one in which most had a three day cycle.  A mosquito that did not delay returning to feed had to oviposit and locate a host that same night.  Thus, they tended to bite later in the night.  When nets were used by the villagers many mosquitoes were unable to feed that night.  Some survived to hunt the next day.  These mosquitoes did not need to lay eggs and were, in all probability, hungry.  They tended to feed earlier in the night.  This then, without any selection taking place, changed the biting cycle to one earlier in the evening.  Maybe this is what is happening to the mosquitoes everywhere they are challenged with mosquito bednets?

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