Gonotrophic Dissociation Research Articles

Diet and Oviposition Deprivation Effects on Survivorship, Gonotrophic Dissociation, and Mortality of Anopheles gambiae s.s.

Diet quality is of paramount importance for egg batch size, longevity, and mortality of vector mosquitoes. Oviposition site presence and absence assumed to be dry season means a lot to the survivorship and mortality of most anthropophilic malaria vectors in sub-Saharan Africa. This study has assessed the effect of different diets and oviposition-site deprivation (OSD) on survivorship, longevity, and mortality of An. gambiae s.s. To determine the effect of diet and OSD on mortality, gonotrophic dissociation rates, longevity, and survivorship, six treatments were employed: Blood Fed with Oviposition (BFO), Blood Fed without oviposition (BF), Blood and Sugar Fed with Oviposition (BSFO), Blood and Sugar Fed without oviposition (BSF), Sugar Fed with Oviposition (SFO), and Sugar Fed without oviposition (SF). Mortality and gonotrophic dissociation were monitored daily. This study found that female mosquitoes offered blood meals with sugar solution and oviposition deprivation survived longer than those deprived of oviposition deprivation. Similarly, female mosquitoes fed on blood and provided with oviposition deprivation lived longer than those without oviposition deprivation. The gonotrophic dissociation rates were found to be lower in groups provided with oviposition deprivation. Our results show that OSD has a direct impact on the survivorship, gonotrophic dissociation rate, and longevity of the malaria anthropophilic vector, An. gambiae s.s., regardless of the diet.

'Nature or nurture': survival rate, oviposition interval, and possible gonotrophic discordance among South East Asian anophelines.

BackgroundMosquito survival, oviposition interval and gonotrophic concordance are important determinants of vectorial capacity. These may vary between species or within a single species depending on the environment. They may be estimated by examination of the ovaries of host-seeking mosquitoes.MethodsLanding collections, Furvela tent-trap and CDC light-trap collections were undertaken sequentially in four locations in Cambodia between February 2012 and December 2013 and samples from the collected mosquitoes were dissected to determine parity, sac stage (indicative of time spent prior to returning to feed) and egg stage.ResultsA total of 27,876 Anopheles from 15 species or species groups were collected in the four locations and 2883 specimens were dissected. Both the density and predominant species collected varied according to location and trapping method. Five species were dissected in sufficient numbers to allow comparisons between locations. Estimated oviposition interval differed markedly between species but less within species among different locations. Anopheles aconitus had the shortest cycle, which was 3.17 days (95 % CI 3–3.64), and Anopheles barbirostris had the longest cycle, which took four days (95 % CI 3.29–4). Anopheles minimus had a higher sac rate in weeks leading up to a full moon but there was apparently little effect of moon phase on Anopheles dirus. Despite the fact that many of the species occurred at very low densities, there was no evidence of gonotrophic dissociation in any of them, even during sustained hot, dry periods. The principal Cambodian malaria vector, An. dirus, was only common in one location where it was collected in miniature light-traps inside houses. It did not appear to have an exceptional survival rate (as judged by the low average parous rate) or oviposition cycle.ConclusionsDifferences in the oviposition interval were more pronounced among species within locations than within species among ecologically diverse locations. A nationwide survey using CDC light-traps for the collection of An. dirus inside houses may help in determining patterns of malaria transmission in Cambodia.Electronic supplementary materialThe online version of this article (doi:10.1186/s12936-016-1389-0) contains supplementary material, which is available to authorized users.

Dry season reproductive depression of Anopheles gambiae in the Sahel

The African malaria mosquito, Anopheles gambiae, is widespread south of the Sahara including in dry savannahs and semi-arid environments where no surface water exists for several months a year. Adults of the M form of An. gambiae persist through the long dry season, when no surface waters are available, by increasing their maximal survival from 4weeks to 7months. Dry season diapause (aestivation) presumably underlies this extended survival. Diapause in adult insects is intrinsically linked to depressed reproduction. To determine if reproduction of the Sahelian M form is depressed during the dry season, we assessed seasonal changes in oviposition, egg batch size, and egg development, as well as insemination rate and blood feeding in wild caught mosquitoes. Results from xeric Sahelian and riparian populations were compared. Oviposition response in the Sahelian M form dropped from 70% during the wet season to 20% during the dry season while the mean egg batch size among those that laid eggs fell from 173 to 101. Correspondingly, the fraction of females that exhibited gonotrophic dissociation increased over the dry season from 5% to 45%, while a similar fraction of the population retained developed eggs despite having access to water. This depression in reproduction the Sahelian M form was not caused by a reduced insemination rate. Seasonal variation in these reproductive parameters of the riparian M form population was less extreme and the duration of reproductive depression was shorter. Blood feeding responses did not change with the season in either population. Depressed reproduction during the dry season in the Sahelian M form of An. gambiae provides additional evidence for aestivation and illuminates the physiological processes involved. The differences between the Sahelian and riparian population suggest an adaptive cline in aestivation phenotypes between populations only 130km apart.

Influence of Multiple Blood Meals on Gonotrophic Dissociation and Fecundity in Aedes albopictus

Gonotrophic dissociation and fecundity in adult female Aedes albopictus affect the transmission of arbovirus and mosquito population dynamics. Female Ae. albopictus bloodfed on guinea pig and human hosts produced significantly (P < 0.05) higher number of eggs (80 and 82/female, respectively) than females fed on chicken (67 eggs/female). Fecundity in mosquitoes that took a double blood meal (chicken and guinea pig), a triple blood meal (3 separate guinea pigs), or mixed blood meals (chicken, guinea pig, and human) was significantly (P < 0.001) higher than in females fed on a single chicken or on 2 separate chickens (refeeding). Gonotrophic dissociation in laboratory colony of Ae. albopictus was first observed and its frequency decreased with multiple blood meals with triple feeding or mixed feeding (3 meals on 3 host types). Blood meal source did not significantly influence gonotrophic dissociation in Ae. albopictus.

2 アカイエカ成虫における栄養生殖分離は適応的形質か?(第57日本衛生動物学会南日本支部大会講演要旨)

2 アカイエカ成虫における栄養生殖分離は適応的形質か?(第57日本衛生動物学会南日本支部大会講演要旨)

Experimental vertical transmission of West Nile virus by Culex pipiens (Diptera: Culicidae).

Despite the detection of West Nile (WN) virus in overwintering Culex pipiens L. in New York in February 2000, the mechanism by which this virus persists throughout the winter to initiate infections in vertebrate hosts and vectors the following spring remains unknown. After a blood meal, parous mosquitoes generally do not survive until spring and gonotrophic dissociation occurs in only a small percentage of the population. To investigate vertical transmission as a means of viral survival during interepizootics, we intrathoracically inoculated Cx. pipiens and Aedes albopictus (Skuse) with WN virus and subsequently tested their F1 progeny for the presence of virus. Among the Cx. pipiens, we recovered virus from two of 1,417 adult progeny that had been reared at 18 degrees C for a minimal filial infection rate (MFIR) of approximately 1.4/1,000 and four of 1,873 adult progeny reared at 26 degrees C (MFIR = 2.1/1,000). The mean titer of the positive pools was 10(5.6) plaque-forming units (PFU)/ml (=10(5.9) PFU/mosquito for positive mosquitoes) of virus. Overall, the MFIR was approximately 1.8/1,000 for Cx. pipiens. Although reports indicate that Ae. albopictus vertically transmit various viruses in the Japanese encephalitis virus complex, we did not detect WN virus in any of > 13,000 F1 progeny of WN virus-inoculated specimens. Female Cx. pipiens that are vertically infected during the late summer season and then survive the winter could serve as a source of WN virus to initiate an infection cycle the following spring.

Evidence of seasonal eggs in Anopheles punctipennis (Diptera: Culicidae).

Anopheles punctipennis (Say), collected in October from resting sites in Illinois, deposited two morphologically distinct types of egg batches. One type was similar to the seasonal "winter" egg of Anopheles walkeri Theobald, with an extensive exochorion that covered all except the tip of the egg. Laboratory rearing of isofemale lines, under two different light-dark and temperature cycles, demonstrated that both types of eggs were intraspecific variants. F1 females from all "winter" egg batches deposited only normal eggs when reared under a 12:12 (L:D) cycle and at 25 degrees C. Most An. punctipennis reared under a 8:16 (L:D) cycle with variable temperature exhibited gonotrophic dissociation or accumulated fat body.

Prehibernation diet and reproductive condition of female Anopheles messeae in Sweden

1. Blood and sugar feeding in the mosquito Anopheles messeae Falleroni were investigated near Uppsala, Sweden, from 1981 to 1985, with emphasis on prehibernation diet. 2. Fructose, indicating plant feeding, was present in females of all ovarian stages, from April to October, and contributed to fat body development in non-gonoactive females before hibernation. 3. An.messeae males and females (inseminated and uninseminated) were observed feeding on floral nectaries of the plants Achillea millefolium L. and Tanacetum vulgare L. at night during August. 4. Gonotrophic dissociation started in some females in July, and by the end of September all females were inseminated and nulliparous but non-gonoactive. 5. Animal sheds were used as diurnal resting sites of non-gonoactive, prehibernating female An.messeae. Among recently fed mosquitoes in that group, 85% were gut positive for fructose and 15% for blood. Most of them showed negative host tropism, indicating that bloodfeeding is not a prerequisite for hibernation. 6. Survival rates of bloodfed (48 +/- 31 days) and non-bloodfed (42 +/- 21 days) females, collected from a cattle shed in September and kept caged without food or water in a store house, were not significantly different. This indicates that bloodfeeding may occur facultatively before hibernation but does not affect longevity and survival. 7. If overwintering is possible for bloodfed An.messeae females, they would be more likely vectors of pathogens such as Batai virus.

Inability of diapausing Culex pipiens (Diptera: Culicidae) to use blood for producing lipid reserves for overwinter survival.

Diapausing Culex pipiens L. females fed 10% sucrose for 7 d following eclosion contained significantly more lipids (P less than 0.05) than nondiapausing females reared and maintained at the same temperature (22 degrees C) but at a longer photophase (14:10 [L:D] instead of 9:15). Diapausing females with limited lipid reserves failed to increase their reserves after blood feeding. The average lipid content of 56 females tested decreased significantly (P less than 0.05) by day 6 after feeding and there was no correlation (r = -0.06) between lipid content at this time and original bloodmeal volumes of individual females. These results refute the contention that blood meals taken by diapausing Cx. pipiens result in fat body development when females are incubated at 18 degrees C during bloodmeal digestion. Diapausing Cx. pipiens with limited lipid reserves were unable to obtain sufficient energy from a single blood meal to survive extended hibernation. Although none became gravid, only 50% remained alive after 20 d in hibernation. In contrast, nonblood-fed females fed only 10% sucrose for 7 to 10 d before being placed in hibernation on a water diet survived for 6 mo with only 50% mortality. There was no evidence for gonotrophic dissociation. Failure of blood-fed, diapausing females to initiate vitellogenesis was correlated with the significantly smaller blood meals taken by most diapausing females and not with hypertrophy of the fat body or temperature during digestion.

Fate of the blood meal in force-fed, diapausing Culex pipiens (Diptera: Culicidae).

Diapausing Culex pipiens L. do not display host-seeking behavior and can be induced to take blood only by being placed in contact with or in proximity to a host for prolonged periods. Such "force-fed" females do not use the blood for lipogenesis, and only some of them use the blood to initiate vitellogenesis. Diapausing Cx. pipiens that are induced to feed eject an average of 4.2-4.6 microliters of blood during overnight feeding periods compared with an average of 0.1 microliters for nondiapausing controls. The reduced avidity of diapausing females for blood, even under optimum conditions, and the ejection by fed females of blood volumes in excess of volumes usually retained indicate that such females are not physiologically programmed for taking and retaining blood. Data for uric acid and hematin excretion and bloodmeal volumes retained by diapausing females are positively correlated with diapause termination and yolk deposition. The occurrence of gonotrophic dissociation need not be invoked to explain the failure of some diapausing females to initiate vitellogenesis following a blood meal. Instead, this is explained by retention of small quantities of blood followed by incomplete digestion and is the expected result of a dose-dependent phenomenon determined by threshold blood volumes. Our data support the concept that the overwintering strategy of Cx. pipiens is limited to gonotrophic concordance in which overwintering females in nature do not take blood or develop eggs until diapause is terminated.

Differentiation of host-seeking behavior from blood-feeding behavior in overwintering Culex pipiens (Diptera: Culicidae) and observations on gonotrophic dissociation.

Host-seeking behavior was differentiated from blood-feeding behavior in overwintering Culex pipiens by comparing engorgement rates in mosquitoes given access to a host in small (0.24-1) and large (3.8-1) chambers. The large chamber requires that most mosquitoes display host-seeking behavior before contacting the host, whereas the small chamber assures such contact by some mosquitoes that are not in a host-seeking mode. Data accumulated in this manner indicate that blood feeding by diapausing Cx. pipiens is rare at simulated late summer and early autumn photophases, even when warmed at 25 °C, unless the host-seeking step is bypassed by placing the mosquitoes near a host. If the host-seeking step is bypassed, some diapausing Cx. pipiens can be induced to feed and some of these may undergo gonotrophic dissociation when incubated at 15 °C and a short photophase during blood meal digestion. However, such feeding followed by gonotrophic dissociation cannot be assumed to occur in nature because host seeking is an essential element in the stepwise series of events preceding blood feeding.

BLOOD-FEEDING AND GONOTROPHIC DISSOCIATION IN OVERWINTERING ANOPHELES EARLEI (DIPTERA: CULICIDAE) FROM SOUTHERN MANITOBA

AbstractA total of 72 overwintering Anopheles earlei Vargas was collected from southern Manitoba during December 1980 and 1981. These mosquitoes were maintained at 15 °or 20 °C, and a photoperiod of 8L: 16D. Forty-two females were offered a blood meal and 25 of these fed. Extensive fat body development was seen in the blood-fed females collected in 1980; this was not seen in collections from 1981. Gonotrophic dissociation was observed in 24 of the blood-fed females.

BLOOD-FEEDING IN OVERWINTERING CULEX TARSALIS (DIPTERA: CULICIDAE) FROM MANITOBA

Diapause development in Culex tarsalis Coquillett has been characterized by reduced blood-feeding to complete termination of ovariole development at or before stage IIa (Bennington et al. 1958; Schaefer and Washino 1970; Schaefer et al. 1971; Bellamy and Corbet 1973; Mitchell 1979). The role that diapausing Culex species have in overwintering arboviruses has been examined (Eldridge 1966, 1968; Eldridge et al. 1972; Reeves 1974; Eldridge and Bailey 1979; Mitchell 1979). Gonotrophic dissociation and its implications for survival of the vector and virus has been reviewed by Washino (1977). Eldridge (1966) indicated gonotrophic dissociation was possible in Culex pipiens L. incubated at low temperature and short daylength and later reported failure of ovarioles of prehibernating C. pipiens to mature following a blood meal (Eldridge and Bailey 1979). Eldridge et al. (1972) reported that Culex restuans Theobald exhibited gonotrophic dissociation in response to conditioning by short daylength and low temperature. Mitchell (1981) has reported blood-feeding and gonotrophic dissociation in a significant portion of diapausing Culex tarsalis from Colorado, when females were kept at 15°C and at short daylength conditions.

Diapause Termination, Gonoactivity, and Differentiation of Host-Seeking Behavior from Blood-Feeding Behavior in Hibernating Culex Tarsalis (Diptera: Culicidae)

Diapausing Culex tarsalis were collected from mine tunnels in Boulder Co., Colorado, during late September and early October 1980 and studied in the laboratory. Exposure to a long photophase (L:D 15:9) resulted in diapause termination in essentially all mosquitoes by day 7 at 25 °C. Warming alone (at 25 °C) for up to 8 days did not terminate diapause in a significant proportion of females maintained at typical autumn day lengths. Diapause was terminated in Cx. tarsalis by topical application of methoprene, a juvenile hormone (JH) mimic, suggesting that the physiological pathway for diapause termination involves secretion of JH by a reactivated corpus allatum. Host seeking and blood feeding were shown to represent discrete stages in the biting cycle of Cx. tarsalis , and these were differentiated in diapausing females by varying the size of the feeding chamber. Diapausing females could be induced to take a blood meal only when the host-seeking step in the biting cycle was bypassed by placing the females in close proximity to a host. Gonotrophic dissociation occurred in a significant proportion of females only when 3 conditions were met: females had to be in a state of diapause when fed, and fed females had to be incubated at a cool temperature (15 °C) and under short-day conditions during the time of blood meal digestion. The demonstration that gonotrophic dissociation can occur under experimental conditions probably has no relation to what occurs in nature. Warm Indian-summer conditions notwithstanding, typically short autumn day lengths are sufficient to suppress host-seeking behavior in diapausing populations and host seeking is a requisite for blood feeding in nature.

Blood-Feeding and Gonotrophic Dissociation in Anopheles Punctipennis (Diptera: Culicidae) Prior to Hibernation in Connecticut

Fifty-six blood-fed and 131 unengorged Anopheles punctipennis females were collected from the basement of a human dwelling in southern Connecticut during late summer and fall 1977. Precipitin tests, conducted on 32 females, disclosed that females had fed on mammals during September and October; host sources included muroid rodent, sciurid rodent, and rabbit. In a separate experiment, 24 of the 56 blood-fed females were confined in plastic cages and maintained on 10% sucrose solution for 2 weeks and, following this period, ovaries were examined to determine stage of follicular development. Since follicles in these females lacked yolk and remained undeveloped, results indicated that gonotrophic dissociation occurred. Examination of spermathecae and ovaries also revealed that each female contained sperm but had not yet oviposited. Anthrone tests, performed on 95 unengorged specimens, revealed that some females acquired nectar in early September. The occurrence of gonotrophic dissociation in this mosquito further increases its vector potential.

The physiological ecology of gonotrophic dissociation and related phenomena in mosquitoes.

The term “gonotrophic dissociation” was originally used to denote the cessation in egg production despite the continued taking of blood meals by overwintering adult anopheline females in a temperate area. A given species may exhibit this phenomenon in some geographical areas, but not in others. In areas where a population displays dissociation, the proportion of blood-engorged females that exhibit this phenomenon may be high. Gonotrophic dissociation is interpreted as an expression of facultative diapause usually induced by short day-length. This paper is intended to review in detail selected papers dealing with the subject of gonotrophic dissociation and related phenomena, make new interpretations based on the most recent studies of reproductive physiology, and finally, to integrate these interpretations and/or conclusions into our present knowledge concerning the physiological ecology of mosquitoes from a more contemporary viewpoint.

Effects of photoperiod and temperature on blood feeding, oögenesis and fat body development in the mosquito, Culiseta inornata

In the laboratory, blood feeding rates, oögenesis and fat body development were utilized to assess the effects of photoperiod and temperature in the conditioning of adult female Culiseta inornata for aestivation. Long-day (16L:8D) and short-day (8L:16D) photoperiods were examined in combination with temperatures of 15°C, 20°C, and 25°C. All tested individuals were reared from egg to adult under one of six possible regimes. Blood feeding occurred in approximately 60% of the females subjected to short-day conditions. Females subjected to long-day regimes exhibited gonotrophic concordance (the inhibition of blood feeding), evidenced by a decrease in overall blood-feeding rate to 20%. Inhibition of blood feeding by long-day females decreased in a linear fashion with increasing temperature. No interaction of the effects of photoperiod and temperature upon blood feeding was apparent. Examination of the ovarioles of post-blood feeding females, reared under each of the above conditions, revealed no evidence of gonotrophic dissociation (the inhibition of oögenesis despite continued blood feeding). Fat body hypertrophy occurred in females reared under long-day conditions, whereas hypotrophy of this tissue was apparent in short-day females. No significant difference in fat body development occurred between parous and nulliparous females reared under long-day photoperiod conditions. Short-day blood-fed females reared at 15°C deposited a significantly greater amount of fat than short-day blood fed females reared at 20° and 25°C, and short-day nonbloodfed females reared at 15°, 20°, and 25°C. The primary stimulus for fat body hypertrophy appears to be long-day photoperiod conditions. Temperature exerted little discernible effect upon this process, and there was no interaction between the effects of photoperiod and temperature upon the degree of fat body development.

Effect of photoperiod and temperature on ovarian development in Culex pipiens pipiens

Culex pipiens pipiens is one member of the C. pipiens complex which diapauses as an adult. Experiments show that photoperiod and temperature both affect the development of the ovarian follicles. Females reared at a 15 hr photophase and 22°C show an increase in follicle size over the first 8 days after emergence. Females reared at 10 hr and 22°C do not show an increase in follicle size. Follicle size does not gradually increase as photophase is lengthened. Rather, at photophases between 9 and 12 hr the follicles remain small and at photophases of 13 hr or more, the increase is seen. An increase in temperature tends to increase follicle size regardless of the photophase. However, a strong interaction between photophase and temperature is evident. No evidence exists for a single ‘critical stage’. Instead, the final follicle size is dependent, in a complex manner, upon the photophase experienced by all the stages. The final size is not a result of a cumulative effect. Photoperiod, independent of temperature, shows a marked effect on blood feeding. Females reared at 15 hr feed much more readily than those reared at 10 hr. Those 10 hr females that feed show no signs of gonotrophic dissociation.

A preliminary study of the seasonal geographic distribution and overwintering of Culex restuans Theobald and Culex salinarius Coquillet (Diptera: Culicidae).

A preliminary study was made of overwintering mechanisms and phenology of 2 common eastern United States mosquitoes: Culex restuans Theobald and Culex salinarius Coquillett. The seasonal distribution of adult activity of the 2 species was established by the month by month plotting of collection records gleaned from 170 published articles. Colonized females of each species were subjected to simulated fall conditions of temperature and photoperiod. C. restuans showed a marked reduction of blood feeding and exhibited gonotrophic dissociation in response to conditioning by short photoperiod and low temperature (15° and 20°C). C. salinarius females showed a significant reduction of blood-feeding under conditions of short photoperiod, but only at the lowest conditioning temperature (15°C) and did not exhibit gonotrophic dissociation. The authors suggest that both species undergo a true diapause but that qualitative and quantitative differences contribute to the generally more northern distribution of C. restuans. The implication of diapause to overwinter survival of arboviruses is discussed.

Physiological condition of overwintering female Anopheles freeborni in California (Diptera: Culicidae).

Studies were carried out on Anopheles freeborni Aitken in the lower Sacramento Valley of California from 1963 through early 1967 to determine the physiological condition of females which survive winter. Overwintering was accomplished by inseminated females that had undergone a reproductive diapause from September through December. Diapause was primarily characterized by the suspension of reproductive activity and buildup of fat body. The proportion of females taking blood during this critical period was low, but females which did so exhibited gonotrophic dissociation. Field studies indicated a strong possibility that decreasing photoperiod rather than low temperature initiated imaginal diapause. This possibility was supported by laboratory studies in which the proportion of long-day females that took blood meals was significantly greater than was the proportion of short-day females that fed. Additional studies with a laboratory colonized strain indicated that temperature also may play an influential part in controlling the onset of diapause.