Biological Rhythm Research 2004, Vol. 35 Nos 1/2. pp. 79–92
Daily Rhythms in Disease-Vector Insects Romina B. Barrozo1, Pablo E. Schilman2, Sebastián A. Minoli1 and Claudio R. Lazzari1,3 1
Laboratorio de Fisiología de Insectos, DBBE, Fac. Cs. Exactas y Naturales, Universidad de Buenos Aires, Argentina; 2Ecology, Behavior and Evolution Section, Division of Biological Sciences, University of California at San Diego, La Jolla, U.S.A.; 3Institut de Recherche sur la Biologie de l’Insecte, UMR CNRS 6035, Université François Rabelais, Tours, France
Abstract The host-vector-parasite interaction offers a clear illustration of the adaptive value of biological rhythms. In this review, we summarise some of the information currently available on daily rhythms of insect vectors, particularly those responsible for the transmission of parasites to humans. Included amongst the cases described are circadian rhythms of locomotor and flight activity, and of eclosion and oviposition in tsetse flies, blood-sucking hemipterans, mosquitoes and other haematophagous insects. Both published and new data are presented, and they indicate that a study of the rhythms in disease-vector insects can provide an understanding of the value of this application of chronobiology to ecology and applied sciences. Related to this, the possibility of strategies for the control of insects based on their temporal characteristics is proposed; for example, the use of insecticides could be restricted to those phases of the day when the susceptibility of the insects to them is increased. Keywords: Disease-vector insects, daily rhythms, activity, oviposition, ecdysis, egg hatching, tsetse flies, blood-sucking bugs, mosquitoes.
Introduction The host-vector-parasite interaction offers a wonderful example of the adaptive value of biological rhythms. The temporal dependence of vector and parasite upon the host has sharpened the fine-tuning of activities, resulting in a precise synchronisation of the three components. In this way, hosts modulate their general activity, usually
Address correspondence to: Claudio R. Lazzari, Institut de Recherche sur la Biologie de l’Insecte, Faculté de Sciences et Techniques, Université François Rebelais, Av Monge — Parc Grandmont, 37200 Tours, France. Tel./Fax: +33 (0)2 47 36 73 89; E-mail:
[email protected] DOI: 10.1080/09291010412331313250
© 2004 Taylor & Francis Ltd.
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according to internal and/or external factors, vectors adapt to the host rhythm for a maximal benefit, and parasites take into account both host and vector rhythms. As pointed out by Pittendrigh (1974), the functional significance of the entrainability of self-sustaining oscillators — in particular, their predictive value and ability of timing under conditions of absence of adequate sensory inputs — can be clearly illustrated with the migration of parasites into the blood stream of their vertebrate hosts. This displacement of parasites towards peripheral blood vessels is timed to match the time when the local insect vector is most actively searching for a host to feed upon. The parasites themselves lack the capacity to perceive the presence of vectors. However, the host’s internal environment provides them with reliable temporal cues which are phased to local time due to the entrainment of the host’s circadian clocks to the light cycle. The migration would be coupled to the appropriate phase of the parasites’ circadian oscillator, assuring their presence under the host’s skin when the vector is actively looking for a blood meal (Pittendrigh, 1974). That time differs among both geographic localities and vector species, but always corresponds with the vector’s feeding time (Pittendrigh, 1974; Hawkins, 1975) (Fig. 1). For the vector, the timing of its activity is the result of the interaction among different factors — notably, the environmental conditions and the resting periods of hosts and predators, which are sometimes different roles played by the same individual. The small size (or high ratio of surface area to volume) of most insects makes them prone to desiccation in dry and hot places or at certain times of the day. It has been found that different species exhibit dissimilar degrees of tolerance to temperature and humidity, colonising more or less discrete spatial or temporal niches (Pittendrigh, 1950). This fact shifts the daily activity of many insects to dusk, dawn or both, i.e., towards the times when the relative humidity reaches its maximal daytime values. This also seems to be the reason why certain processes — even those occurring just once or only a few times during the insect’s life, such as egg hatching or ecdysis — for which low relative humidity is deleterious take place at sunrise (Ampleford &
Figure 1. Synchronisation between the migration of microfilaria into the blood stream of hosts and the biting activity of their vectors in different geographic areas. The number of parasites in the peripheral blood vessels is depicted as a function of time (redrawn from Aschoff, 1989).
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Steel, 1982; Lazzari, 1991; Schilman, 1998). The rhythmicity in such processes, either unique or sporadic, becomes apparent only at the population level. Finally, host activities are scheduled by many factors, among these being resource exploitation and the avoidance of predation and parasitism. As already mentioned, host temporal organisation will shape the activity of vectors and also of the parasites associated with both, creating a complex circle of temporal interactions. Much attention has been paid to the temporal organisation of man and mammals, and relatively less to insect vectors. Although the study of temporal organisation of parasites is far more difficult from an experimental point of view, highly relevant information has been obtained by several investigators. The present review summarises some of the information available about the second component of this fascinating chain of interactions — the insects responsible for the transmission of parasites to their hosts, particularly to humans.
Tsetse Flies Daily rhythms have been observed in a wide variety of behavioural, physiological, and metabolic processes in several insect vectors. Individuals maintained under natural or artificial cycles of light and/or temperature express spontaneous daily activity patterns, primarily restricted to a particular time period during the day. Activity is frequently bimodal, with peaks occurring near dawn and dusk. This is particularly clear, for example, in the tsetse fly Glossina morsitans (Brady, 1972), the vector of the African trypanosomiasis, where the same bimodal pattern has been observed in the field, as biting activity, as well as in the laboratory for different behaviours (Fig. 2).
Figure 2. Daily activity pattern of tsetse flies, Glossina morsitans. Ordinates represent percentage deviations from the mean (redrawn from Brady, 1975).
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Tsetse flies are diurnal haematophagous (blood-eating) insects that feed mainly during the early morning and late afternoon (Brady & Crump, 1978). In laboratory studies, G. morsitans exhibited morning and evening peaks of spontaneous flight activity, with low activity around midday and none during the night (Brady, 1972). This typical profile of flight behaviour, observed under a 12 : 12 h light/darkness cycle is partially affected by temperature, but could not be explained as negative masking by temperature around noontime. Although the amplitude of the rhythm changes according to temperature, bimodality persists at different temperatures (Brady & Crump, 1978). According to these authors, temperature would be responsible for 20% of the variation in the intensity level of the response during the day, while 80% would be of endogenous origin. The rhythmicity of tsetse flies is also affected by other factors. The bimodal pattern of flight activity is not retained under constant darkness, where a single-peaked, unimodal rhythm appears (Brady, 1988). Under this condition, the physiological state of the flies affects the timing of the single activity peak. In this way, mature flies (i.e., fed several times) exhibited a peak at subjective dusk, whereas ‘teneral’ flies (unfed, recently emerged) do so at subjective dawn (Brady, 1988). These results have been explained as the result of a physiological switch occurring in response to the first blood meal. Daily rhythms of responsiveness to different sensory stimuli have also been reported in tsetse flies. When stimulated with host-associated odours or visual stimuli, tsetse flies showed a daily bimodal pattern of responsiveness, with peaks at dawn and dusk (Brady, 1975). Furthermore, the chemoreceptors located on the antennae of G. morsitans and G. fuscipes also responded to host-related stimuli with a daily rhythm in synchrony with much of its behavioural repertoire (Van der Goes van Naters et al., 1998). Several other examples of rhythmic behaviour have been reported in these insects. Brady (1975) described the daily dynamics of resting, defaecation and probing responsiveness. It is worth noting that all the rhythms described in these insects appeared to match the pattern of spontaneous flying activity described by Brady (1972) (Fig. 2).
Blood-Sucking Hemipterans One of the first descriptions of daily rhythms in haematophagous bugs refers to the bedbug Cimex lecturarius. Although these insects have not been linked to transmission of any disease to man, they have been shown to harbour the causative organisms for several infections. Controlling bedbugs has been a challenge to people for centuries, since saliva injected at the time of feeding is associated with local and sometimes widespread urticaria. By placing traps in an animal room infested with bedbugs, Mellanby (1939) studied the activity of these insects. This author established that they were most active between 03:00 and 06:00 h, the rhythm apparently being endogenous (Cloudsley-Thomson, 1961). It is worth noting that, although the hosts were resting and motionless throughout the night, the bugs only became active at dawn, i.e., when the relative humidity reaches its maximum daily level.
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Triatomine bugs, vectors of the American trypanosomiasis or Chagas disease, are usually described as having typically nocturnal habits. Their life exhibits a high degree of temporal organisation and different processes have been described to be temporally-modulated. The expression of some of these processes can be observed at the individual level (e.g., locomotor activity), whereas the occurrence of others only becomes evident when whole populations are analysed (e.g., eclosion). In contrast with tsetse flies, where the typical V-shaped (bimodal) curves recur for different activities, in Triatoma infestans, every process occurs with a particular temporal pattern, different activities being manifest in discrete temporal windows (Fig. 3). Table 1 summarises the information available about temporal organisation from studies conducted mainly on T. infestans and Rhodnius prolixus, but also upon some other members of the more than 130 species of triatomines that have been described. Dispersion, leaving refuges, enhanced response to host odours, food search, oviposition, flight initiation, enhanced phototactic sensitivity, dark adaptation of compound eyes and ocelli, preference for environments with relatively high temperature, and attraction to beta-light (long lasting chemically produced light using a radioactive element) have all been shown to take place at the beginning of the night. By contrast, aggregation, ecdysis, egg hatching, refuge entering, and preference for relatively cold places occur at dawn. During the hours of daylight, when the bugs remain inactive in groups, the phototactic sensitivity is relatively lower, and the visual system (of both simple and compound eyes) is adapted to ‘light’ conditions. Locomotor activity occurs at dusk and dawn, following a bimodal pattern. Under DD conditions, T. infestans continues to show this bimodal pattern, thus evincing the endogenous nature of both components of the rhythm. However, it becomes unimodal when the insects are maintained under a LL regime (Lazzari, 1992). Several of these rhythms are probably controlled in the same way. The temporal occurrence of activity peaks and the timing of leaving/entering refuges have been shown to be related to searching for food and refuge at dusk and dawn, respectively (Lorenzo & Lazzari, 1998). The motivation to feed at the beginning of the night correlates well with the increased attraction to a host’s odour (carbon dioxide) at the same time (Barrozo, 2003). On the other hand, the apparently obvious relationship between the circadian rhythm of phototactic sensitivity (Reisenman et al., 1998) and that of light/dark adaptation of the compound eyes (Reisenman et al., 2002) is only indirect; whereas the former is expressed under both DD and LL, the latter vanishes in LL. The phenomenon, in triatomines, of splitting activities into discrete temporal windows is not only clearly evident for certain activities (e.g., searching for food when the hosts are resting) but also has an obvious adaptive value, since active hosts become potential predators. It has also been postulated that the circadian control of ecdysis and egg hatching, both processes occurring at dawn, could be related to the maximum values of environmental relative humidity (RH) occurring at this time of the day (Ampleford & Steel, 1982; Lazzari, 1991; Schilman, 1998). In this way, the bugs, particularly those species that exhibit a preference for dry environments, would avoid drier periods, which could diminish the success of eclosion (Roca & Lazzari, 1994; Schilman, 1998; Lorenzo & Lazzari, 1999; Guarneri et al., 2002). It can be
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Figure 3. Daily profile of different processes in Triatoma infestans. a, locomotor activity; b, use of refuges; c, feeding activity; d, egg hatching; e, thermopreference; f, responsiveness to carbon dioxide. (In all cases, redrawn from original data by the authors).
high few few high high high high high darkness darkness high high outgoing attraction
Locomotor activity Ecdysis Egg hatching Dispersion Oviposition Motivation to feed Responsiveness to carbon dioxide Photonegative sensitivity Adaptation of compound eyes Adaptation of simple eyes Preferred temperature Flight activity Refuges related activity Response to beta-light
low few few high low mid low high darkness darkness mid none out/in none
Middle
Night
high many many low low low low high darkness darkness low none incoming none
Late/Dawn none few few assembling none low low low light light low none none none
Day TC TC TC ? TC ? TC TC TC TNC TC ? ? ?
*Class of rhythm References
Constantinou (1979); Lazzari (1992) Ampleford & Steel (1982) Lazzari (1991) Lorenzo Figueiras et al. (1994) Constantinou (1984); Ampleford & Davey (1989) Lorenzo & Lazzari (1998) Barrozo (2003) Reisenman et al. (1998) Reisenman et al. (2002) Fischbein (2003) Minoli & Lazzari (2003) McEwen & Lehane (1993) Lorenzo & Lazzari (1998) Bertram (1971)
*TC = truly circadian (endogenous); TNC = truly non-circadian (direct response to environment).
Dusk/Early
Daily rhythms in Triatominae bugs.
Process
Table 1.
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hypothesised that these bugs have a temporal strategy — to avoid low RH at eclosion time — rather than a spatial one. As mentioned above, many morphological, physiological and behavioural processes in these insects have been shown to change during the course of the daytime. For almost every daily rhythm analysed in detail in triatomines, an endogenous component has been conclusively demonstrated. This is the case with the rhythms of locomotor activity, egg hatching, oviposition, ecdysis, sensitivity to light, sensitivity to certain host odours, thermopreference and light/dark adaptation of compound eyes. These can be considered true ‘circadian’ rhythms (Constantinou, 1979; Ampleford & Steel, 1982; Ampleford & Davey, 1989; Lazzari, 1991, 1992; Reisenman et al., 1998, 2002; Minoli & Lazzari, 2003; Barrozo, 2003). The only exception to this rule that has been found so far is the light/dark adaptation of the simple eyes or ocelli (Fischbein, 2003). Astonishingly enough, the two visual systems that coexist in the same individuals are controlled in different ways. Probably, the non-circadian regulation of the adaptation of simple eyes is related to the measurement of the absolute intensity of the light in the environment, and is assessed without any adjustment in sensitivity or pre-adaptation evoked by a clock. Other rhythms, such as those of flight initiation, refuge incoming/outgoing and feeding motivation, have not yet been tested for endogeneity (McEwen & Lehane, 1993; Lorenzo & Lazzari, 1998). Experimental studies of the locomotor activity of T. infestans have revealed that multiple oscillators, organised in a hierarchical fashion, control the circadian activity of triatomines (Lazzari, 1992). The two spontaneous bursts of activity, displayed during the first hour of the scotophase and at the beginning of the photophase, have been shown to be under the control of two different endogenous oscillators, each exhibiting its own period of spontaneous oscillation under constant conditions and having a different sensitivity to light. The locomotor activity of T. infestans has been shown to be synchronised by light as well as temperature cycles. When tested separately, the latter Zeitgeber exhibited the higher synchronisation power, in agreement with the high thermal sensitivity of this species. However, when offered together at different phase relationships, light cycles dominate temperature cycles, evincing a relative hierarchy between light- and temperature-driven oscillators that favours the environmental cue which has the better signal/noise ratio, i.e., the daily light/dark cycle. These oscillators are affected by different factors (e.g., temperature level) or manipulations (e.g., antennectomy), which mask or modulate their expression (Lazzari, 1992). The temporal organisation of triatomine life has not been yet exploited by vectorcontrol programs. As described above, the proportion of individuals out from their refuges is maximal at dawn. Moreover, at the same moment, many of them have just fed, or are active, moulting or hatching. High metabolic rates produced by activity, the changes in cuticle permeability that take place at feeding or at ecdysis, and the exposure of individuals to open places, are all conditions that favour exposure of insects to insecticides and the penetration of these substances into them. Therefore, according to the temporal organisation of triatomine life, daybreak appears to be the best time for spraying a more vulnerable insect.
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Mosquitoes Some of the most deadly and widespread diseases in the world are transmitted by mosquitoes. Different species are vectors of malaria, yellow fever, dengue, encephalitis, filariasis and other infections. Many investigations have shown the existence of circadian rhythms underlying several physiological processes in these insects (Jones, 1976, 1982; Chiba et al., 1993; Shinkawa et al., 1994). Furthermore, it has been shown that such biological rhythms could be affected by many internal and/or external factors, such as reproductive and developmental state, temperature, light intensity, etc. Mosquitoes have provided a valuable model system for the experimental analysis of these processes. In the mosquito Culex pipiens, the flight activity pattern is clearly bimodal when the insects are maintained under light/darkness cycles. Under DD conditions also, insects continue to show a bimodal pattern, thus indicating the endogenous nature of the rhythm. However, flight activity becomes unimodal when the insect is maintained under an LL regimen (Jones, 1976) or exposed to increasing light intensity (Jones, 1982). Patterns of activity, or even the expression of rhythmic behaviour of female mosquitoes, can also be affected by their reproductive state (i.e., insemination), bloodfeeding condition and egg maturation (Jones et al., 1972; Jones & Gubbins, 1978, 1979; Jones, 1982; Rowland, 1989). Species so far studied include the crepuscular and nocturnal Anopheles gambiae, A. stephensi and C. quinquefasciatus (Jones & Gubbins, 1978; Jones, 1982; Rowland, 1989) and the diurnal Aedes aegypti (Jones, 1981). In nocturnal mosquitoes, males and females under LD cycles synchronise their activity pattern, with a maximum at dusk. The peak is concentrated and precisely timed, a result that might ensure co-ordination of the timing of activity in the two sexes (Jones & Gubbins, 1978). Male responsiveness to the female flight tone is limited to the initial peak (dusk) by a circadian rhythm of erection of the fibrillae of their antennae (Nijhout, 1977). Virgin females exhibit the two characteristic peaks of activity at dawn and dusk. Blood-feeding has little effect on the activity patterns of these virgin insects, which remain active mainly at dusk, independent of their nutritional state, probably searching for a mate. In contrast, blood intake affects the activity levels in inseminated female mosquitoes. When unfed, they are active throughout the night whilst, after feeding, they decrease their activity during the first two nights, resuming their previous activity level when oocytes are mature. This change in the activity pattern might be related to the search for a suitable oviposition site (Jones & Gubbins, 1978; Rowland, 1989). The alteration in temporal pattern of activity of inseminated females is caused by a factor produced in the male accessory gland (Jones & Gubbins, 1979; Chiba et al., 1990). Regarding the rhythms from an evolutionary standpoint is important in order to compare phylogenetically closely related species that occupy different environmental habitats. Mosquitoes appear to be good models for this kind of study. For example, Shinkawa et al. (1994) analysed the variability in the activity pattern (flight and walking) in strains of C. pipiens molestus from Iran, Egypt and two localities of Nagasaki (Japan), as well as of C. pipiens pallens, also from Japan. C. pipiens moles-
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tus has evolved from C. pipiens pipiens, after invading highly polluted water in underground habitats that frequently have restricted human access and low intensities of light. Shinkawa et al. (1994) found that both species exhibited two peaks (i.e., at lights-on and lights-off) and additional activity during the dark period. During the photophase, only females of the Iranian and both Japanese molestus strains continued to show a basal activity level. When tested under constant darkness conditions, all strains maintained the rhythm of activity, each with its own period, demonstrating that an endogenous component was involved in such behaviour. That is, differences have been found in daily and circadian properties of the activity rhythm not only between C. pipiens pallens and C. pipiens molestus, but also among strains of C. pipiens molestus. In addition, the latter strains exhibited the second shortest free-running period (measured under DD conditions) known in insects, i.e., about 21 h (Shinkawa et al., 1994). Mosquitoes show a diverse temporal pattern of oviposition: some are diurnal while others are nocturnal; and some present an unimodal shaped curve while, for others, it is bimodal (e.g., Chadee & Mohammed, 1996; Chadee & Beier, 1996; Chadee et al., 1998; Corbet & Chadee, 1990). In addition to the multiple effects on host behaviour described for parasites, a modulation of daily activity seems to be present in mosquitoes, although opposite effects have been found in different species. Thus, in Anopheles stephensi, the flight activity fell to about 67% of control levels when parasitised with the rodent malaria causative agent, Plasmodium yoelii (Rowland & Boersma, 1988); by contrast, Anopheles trivittatus exhibited an increase in flight activity when infected with Dirofilaria immitis (Berry et al., 1988). However, in both cases, the circadian activity pattern was not affected by the parasitism. In these studies, no attempts to verify the existence of an endogenous clock were carried out; thus it is not known if these are true circadian rhythms. Microfilariae of various filarial worm species have adapted to the biting behaviour of their vectors, by displaying circadian periodicity in their density in the host’s peripheral blood. Thus, the microfilariae attain their highest density in peripheral blood at the time when their corresponding vectors show their peak of biting activity (Hawking, 1975; Simonsen et al., 1997). However, it is not yet clear whether other parasites possess the same strategy. Investigations by several authors of human malaria infection with Plasmodium falciparum (Hawking et al., 1971; Githeko et al., 1993; Magesa et al., 2000), could not convincingly demonstrate the existence of linked circadian periodicities in the blood density of parasites and the biting activity of the local vector Anopheles gambiae (Magesa et al., 2000).
Other Haematophagous Insects Fleas are not only annoyances for humans and domestic animals, but they also transmit a myriad of bacterial species including notable pathogens. A circadian rhythm of locomotor activity (i.e., jumps and runs) was found by autocorrelation analysis in newly-emerged individuals of the flea Ceratophyllus sciurorum (Clark et al., 1997). The persistence of a 24-h rhythm under constant conditions (DD) gives a strong indi-
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cation that the flea has an endogenous clock controlling its activity. Moreover, feeding affects the expression of the rhythm (Clark et al., 1999). A significant difference in activity becomes apparent when comparing the number of hours of activity between fed and unfed fleas, this number being increased in the latter. Thus, the rhythm adjusts in hungry fleas to increase the chance of encountering a host. Black flies, members of the Simuliidae family, are haematophagous insects. They transmit parasites from host to host via the blood meal, affecting many people in West Africa and Central America. Biting and flying activities in these insects appear to vary according to the time of the day. However, whilst some authors found that certain species of black flies exhibit a bimodal pattern, with peaks of biting during the early morning and the late afternoon (Renz, 1987), other authors found a unimodal curve in other species (Davis et al., 1994). The chronobiological basis of the activity patterns in many black flies has not been studied yet (Sutcliffe, 1986). Although some data are available from the univoltine Prosimulium kiotoense, which lay most eggs at mid-day (Baba & Takaoka, 1991), no analysis of endogenicity has been carried out regarding the ovipositional habits of black flies.
Final Remarks Insects are excellent models for chronobiology, as demonstrated in seminal works conducted by pioneers of the study of biological rhythms. They can be easily reared in the laboratory, have short generation-times, and are robust for experimental surgical manipulation (e.g., ligatures, decapitation, transplantation, parabiosis). Moreover, the study of disease-vector insects has the potential advantage to applied science of providing basic knowledge on the temporal organisation of pests’ lives. This information can greatly improve the control of disease vectors by traditional methods like insecticides, by applying them during times of higher susceptibility — for example, when ecdysis or hatching take place and the body cuticle is most permeable. The authors hope that the information summarised here will encourage chronobiologists and medical entomologists to conduct work in this area.
Acknowledgements The authors wish to express their gratitude to the editors for improving the text. This work received financial support from the UNDP/World Bank/WHO Special Programme for Research and Training in Tropical Diseases (TDR), CONICET, and the Universidad de Buenos Aires (Argentina).
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