In contrast to temperate and subtropical zones, seasonal patterns of parasite relapse in parasites such as
P. vivax and
Hepatocystis spp. (tropical relatives of
Haemoproteus infecting baboons) in the tropics is less evident and thought not to occur [
29]. Unlike temperate zones, seasons in the tropics are based largely on rainfall and are, therefore, intimately linked to mosquito bionomics. Given this intimate link between season, mosquitoes and transmission, how can seasonality in
P. falciparum be detected? As stated previously, current wisdom holds that there is a continual production of low numbers of gametocytes that are the source of infection once mosquito numbers expand. However, contrary to accepted belief, mosquitoes can be found at all times of the year, even under very hostile climatic conditions [
30] and seasonal mosquito activity is, therefore, primarily one of greatly increased numbers. Thus, as an initial test of transmission seasonality, the occurrence of infected "out of season" anophelines is examined. The traditional explanation for the absence of infections in anophelines is that climatic conditions reduce the lifespan of the adult mosquitoes such that the probability of their surviving long enough to allow completion of sporogonic development is negligible – that is, the vectorial capacity [
31] is considerably reduced by the decreasing vector longevity. However, by examining the mosquito for oocyst (midgut) as well as sporozoite (salivary gland) infections, the extent of human infectiousness can be established irrespective of whether there is actual transmission. Bentley (1911) [
32] summarizes several studies of this nature where anopheline stomachs and salivary glands were examined on a seasonal basis (Table
1). Although admittedly very limited, these data argue against a persistent level of human infectiousness to mosquitoes.
Table 1
Comparison of the oocyst and sporozoite rates in mosquitoes sampled during the non-transmission and transmission seasons. Data from Bentley (1911) [32].
Bentley 1911 | Bombay | Nov-June | 178 / 123 | 0 | 0 |
| | July-Oct | 659 / 703 | 12.7 | 4.1 |
Gosio 1905 | Tuscany | Apr-June | 318 | 0 | 0 |
| | July-Oct | 512 | 27 | 4 |
Daniels | British Central Africa | Dry season | 1500 | 0 | 0 |
Such anopheline data are one side of the coin and gametocytes are the other. If tropical seasons are defined most precisely by mosquito bionomics, it is conceivable that
Plasmodium spp. would have evolved to respond to the mosquitoes themselves. Thus, in a manner akin to temperate parasite species that utilize vertebrate host seasonal cues to produce gametocytes at the optimal time, tropical species may respond to tropical cues – the mosquito bites. Is there any evidence that
P. falciparum, for example, produces gametocytes in response to mosquito bites? As with
P. vivax,
P. falciparum gametocyte production has been found to peak at a time when the anopheles abundance was at a maximum [
33‐
35]. However, this peak gametocyte rate occurred notably after the peak in the number of clinical cases and, thus, after the peak in transmission. Such an increase in gametocyte rate would be expected as a result of novel infections and, thus, characteristic of an endemic region during the transmission season. However, what evidence is there that, at the beginning of the transmission season, there is an increase in infectiousness of humans to mosquitoes that is not due to novel infections, but due to relapses in existing chronic infections. Identifying the human reservoir of infection and correlating gametocyte density with transmission success to mosquitoes is far from clear [
36]. The human reservoir of infection (during the non-transmission season) will depend on the rate of recovery from infection, which in turn depends on the extent of previous exposure and the immune reaction to infection. Both these factors will alter with age for a given intensity of transmission. Therefore, in the absence of novel infections, the human reservoir of infection will have an age-specific distribution. If mosquito bites are having a gametocyte-promoting effect on existing chronic infections, then age-specific patterns of gametocyte production might be expected. However, although increasing gametocyte density tends to result in greater infectiousness to mosquitoes [
19,
37,
38], it has been repeatedly demonstrated that high gametocyte densities do not guarantee high mosquito infection rates [
19,
38‐
40]. Cryptic infectors with no or very few apparent gametocytes, are capable of infecting mosquitoes and may contribute to a very significant proportion of the human transmission reservoir [
39‐
41]. Moreover, gametocyte density varies greatly according to the region of study, and also with age (i.e. history of exposure) of the individual and tends to reflect the overall asexual parasite density [
42,
43]; consequently, infections in the younger and therefore less immune individuals tend to produce higher densities of gametocytes [
44‐
46] than adults. Therefore gametocyte density itself may not be a sufficiently sensitive indicator. Rather, age-specific seasonal changes in intra-host parasite prevalence rates are preferred. This measure encompasses changes in both sexual and asexual prevalence rates and the tendency for an infection in a particular age group to produce gametocytes; it is, thus, a measure of parasite behaviour within a particular age-group during a certain season. To examine the potential role of mosquito bites on the seasonal nature of
P. falciparum transmission, three historical data sets, addressing age-specific longitudinal patterns of
P. falciparum asexual and sexual prevalence rates in relation to mosquito abundance patterns, are analyzed. One of the major shortcomings of these studies is that they did not have recourse to PCR (quantitative, reverse transcriptase) technology and thus will have underestimated parasite prevalence rates and can not distinguish a relapsed chronic infection from a novel infection. However, despite such limitations, the data sets reveal much on the seasonality of
P. falciparum transmission.