Evaluation of Aedes aegypti sugar feeding behaviour in a semi-field system in Tanzania

doi:10.21203/rs.3.rs-2213540/v1

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Evaluation of Aedes aegypti sugar feeding behaviour in a semi-field system in Tanzania

https://doi.org/10.21203/rs.3.rs-2213540/v1

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Background

Sugar feeding behaviour is an essential aspect for mosquito survival, fitness, reproduction, and competence. Understanding the behaviour of Aedes aegypti is a fundamental phenomenon for the development of new interventions for controlling the vectors. The objective of the current study was to investigate i) the time in an Ae. aegyptimosquito’s adult life when they are most likely to sugar feed ii) if sugar sources availability limits Ae. aegypti blood feeding with the aim of informing control strategies using attractive-targeted sugar baits (ATSBs)

Methods:

The preference of Ae. aegypti to feed on sugar or blood and the effect of sugar source availability on Ae. aegypti blood feeding was studied at different chronological and physiological ages in semi-field conditions in Bagamoyo, Tanzania. Experiments were done through a series of paired–choice assays whereupon mosquitoes were allowed to choose between a sugar meal or a blood meal in the form of a rabbit.

Results

In the first five days post emergence, Aedes aegypti mosquitoes were equally likely to opt for a sugar meal or a blood meal. However, after the first gonotrophic cycle Ae. aegypti prefer to feed on blood meal (OR=9.4; 95%CI= [6.7-13.0]; p<0.001) over a sugar meal (OR=1). Moreover, a nulliparous Ae. aegypti mosquitoes are less likely to blood feed if they have both sugar and blood sources available (OR=0.06; 95%CI [0.02-0.16] p<0.001).

Conclusion

In this study, sugar meal is observed to be a part of Ae. aegypti life particularly at the younger stage (nulliparous stage). Therefore, there is potential for the development of interventions such as attractive toxic sugar baits (ATSBs).

Attractive-targeted sugar bait

Aedes aegypti

sugar-feeding behaviour

blood-feeding behaviour

mosquito ecology

Tanzania.

Mosquitoes of both sexes feed on sugar from plants and honey dews for survival, flight, and mating purposes. Aedes is among the mosquitoes responsible for the transmission of viral diseases such as Dengue fever and Chikungunya. And the control of the diseases relies on the control of mosquitoes. Therefore, knowing the sugar-feeding behaviour of Aedes mosquitoes is an important aspect for the development of an intervention such as sugar bait that attracts and kills the mosquitoes. In this study, we investigated Aedes aegypti sugar and blood feeding preferences just after emerging and after the first eggs cycle by giving them a choice between sugar and blood meals in the same cage. The results show that Aedes mosquito does not differ in feeding preference between sugar and blood meals in the first five days post emergence. However, after the first eggs cycle, the majority of the mosquitoes prefer to take blood meal over sugar meal followed by a mixed meal. Also, we observed that, the presence of sugar meal reduces the mosquito blood feeding preference. The findings, highlights that sugar bait may be regarded as potential intervention against Aedes mosquitoes when are at younger stage than older stage.

Both male and female mosquitoes feed on sugar sources from plants and honeydews for survival, fitness, and fecundity enhancement [1]. Male mosquitoes solely rely on sugar for survival [2]. While male mosquitoes exclusively feed on sugar, females feed on both sugar and blood [3]–[5]. They quest sugar for energy supply and blood for egg development[6], although it has also been shown to increase their survival time [6], [7]. In some mosquitoes species, the sugar intake varies according to mosquito stages (nulliparous and parous stage) [8], [9] highlighting that energy requirement is a life cycle dependent phenomenon.

While sugar feeding is a mandatory phenomenon for mosquito lives [1], it is not the case for female Ae. aegypti. Female Ae. aegypti have been reported to exclusively feed on blood and use it for energy supply as well as egg nourishment [7]. The adaptation is explained by the unusual behavior of mosquito species to frequently imbibe multiple blood meals [10]. The ability to multiple blood feed is reported to have a fitness advantage [11], [12] as well as reproductive output [12]. The combination of advantages has profoundly led the mosquito species to thrive and spread throughout the world. In addition, mosquito blood feeding frequencies have an epidemiological impact in arboviruses transmission because vector biting rate is a fundamental function of vectorial capacity.

Although female Ae. aegypti seem to rely on blood for energy supply, this exclusivity is questionable. Studies researching the Ae. aegypti feeding ecology showed that blood feeding exclusivity is a function of sugar availability, in sugar rich environments, Ae. aegypti will sugar quest for sugar regardless of the presence of blood sources[13], [14]. On other hand, [15] reported the poor egg development when females were deprived of sugar, indicating that the carbohydrate source may actually be a dietary requirement of the female mosquito. Evidence indicates that Ae. aegypti are not exclusive blood feeders but rather that their dietary choices are dependent of their environment. This study indented to investigate the feeding choices of female Ae. aegypti along its adult life and how these may be affected by the availability of dietary resources.

Mosquitoes

All experiments were conducted at Ifakara health institute Bagamoyo using a disease-free insectary-reared Ae. aegypti. The mosquitoes were reared at 27 ± 2⁰C and 75 ± 20% humidity at Ifakara Health Institute insectary in Bagamoyo Tanzania. Larvae were fed with Tetramin® fish food while adults were maintained with 10% w/v sugar solution with natural light regimen. For egg laying, female Ae. aegypti aging 3–6 day old were fed with cow blood through a membrane.

Experiment 1- Aedes aegypti meal choice in the constant presence of sugar and blood sources up to 5 days post emergence

Aedes aegypti’s choice to sugar feed on a sugar bait or blood meal over their life progression was investigated over a period of 5 days post emergence in semi-field conditions. Experiments were done inside an experimental hut within a screened semi-field system (SFS) located at Ifakara Health Institute, Kingani Bagamoyo [16] from October to December 2018. The experimental hut consisted of an Ifakara hut [17] covered with a thatch roof. The inside of the hut was lined with netting with a zip opening at the door.

Five metal-framed cages (120cm x 120cm x 102cm) with removable netting panels and plywood base were placed inside the modified hut. One panel of each cage had a long sleeve which enabled the study team to release mosquitoes into the cage and collect them using an aspirator. A rabbit with shaved back was held inside a smaller cage (60cm x 60cm x 60cm) placed within the larger metal cage. The rabbit’s holding cage was made of wood with wire mesh panels large enough to allow mosquitoes to freely fly in and out of the wooden cage that had the rabbit so that the mosquitoes had a constant availability of sugar and blood sources throughout the experiment.

Five attractive sugar baits (ASBs) without a toxicant were made as per [18]. A stock sugar solution (10%w/v) was prepared and divided into two portions: one dyed with a blue non-toxic food colouring dye (0.5%v/v) and the other with a green non-toxic food colouring dye (0.5%v/v). Each cage was assigned an experimental time-period: Cage I- 24 hours; Cage II- 48 hours; Cage III – 72 hours; Cage IV − 96 hours; and Cage V − 120 hours. Forty freshly emerged female Ae. aegypti (blood and sugar naïve) were introduced into each of the five cages and maintained in each cage throughout its respective experimental time-period. A green dyed ASB was kept inside each cage until 24 hours prior to each cage’s respective experimental time-period and at that point replaced with the blue dyed ASB (Fig. 1). The following day all mosquitoes were collected using a Prokopack aspirator [19], killed in a freezer for 30 minutes, and observed for feeding status which was done by squeezing their abdomens on a white filter paper and noting either the presence of food dye or blood – blue dye -fed on sugar within the last 24 hours; green dye – fed on sugar more than 24 hours ago; or blood fed. At end of each cage’s experimental time-period the rabbit was returned to the animal nursing house. The cage was thoroughly cleaned and left for the next experimental replicate. A total of eight experimental replicates were performed during which the rabbits were rotated between the cages to avoid bias caused by differential mosquito attractiveness between different rabbits.

Experiment 2 - Aedes aegypti meal choice after first gonotrophic cycle

Aedes aegypti sugar and blood feeding preference after the first gonotrophic cycle was investigated in a semi-field conditions as described above at Ifakara Health Institute Bagamoyo [16]. In the insectary, 3-day old Ae. aegypti were blood fed on cattle blood through a membrane feeding system. From these mosquitoes, 150 fully blood fed mosquitoes were transferred into a 30cm x 30cm x 30cm holding cages and maintained in insectary conditions for 48 hrs for effective blood digestion after which they were transferred in batches of 50 into large cages (120 cm x 120 cm x 120 cm) containing a rabbit (Fig. 2) and a sugar source in form of a green-dyed ASB. Oviposition bowls were placed in each of the three large cages. Mosquitoes in each cage were observed for oviposition. Upon observing the presence of eggs, the green dyed ASBs were replaced with blue-dyed ASBs and left for 24 hours. After 24 hours mosquitoes from each cage were collected using a Prokopack aspirator [19] killed in a refrigerator for 30 mins and observed for feeding status by squeezing their abdomens onto a white tissue paper. The number of sugar- fed and blood fed mosquitoes were counted. A total of ten replicates were performed.

Experiment 3 - Effect of limiting sugar availability on Aedes aegypti blood feeding behaviour

Three large cages as described in previous experiments were used to determine if limited sugar availability would affect blood feeding of nulliparous Ae. aegypti. In each set of cages, 40 blood naïve, starved (6–8 hours) Ae. aegypti females aged 3–7 days, were released into each of the three cages. In the first cage an ASB was placed inside but no rabbit, in the second cage a rabbit was placed inside it but no sugar source and in a third cage both rabbit and ASB were made available for mosquitoes to feed on. The mosquitoes were allowed to choose their meal of choice: sugar meal, blood meal or both meals and 24 hrs post release they were collected using Prokopack aspirator [19], and observed for feeding status by squeezing the abdomens as described earlier. A total of ten replicates were performed with changing the positions of the cages after every replicate to avoid potential sources of bias.

Data analysis

All data obtained were analysed using STATA package version 13 (Stata corp, College Station, TX).

Experiment 1 - Aedes aegypti meal choice in the presence of sugar and blood sources up to 5 days post emergence

A generalized linear regression model with logit link was performed to determine the difference in proportion of mosquito sugar or blood fed within the first five days post their emergence. A proportion fed mosquitoes (sugar fed, blood fed and those which fed on both meals) were considered as dependent variables while meal type was regarded as independent variable. Replicates (experimental days) and cage position were treated as covariates. Odds ratios and 95%CI were obtained from the model.

Experiment 2&3 – Aedes aegypti meal choice and the effect of sugar sources availability on blood feeding before and after first gonotrophic cycle.

A descriptive analysis and logistic regression were performed to compare the percentage mean of sugar fed, blood fed and mixed fed mosquitoes at 95% confidence interval before and after first gonotrophic cycle. The Odds ratios at 95% confidence interval were estimated from the models.

Experiment 1 - Ae. aegypti meal preference at different age stages

The proportions of Ae. aegypti mosquitoes which fed on blood only, sugar only and mixed meals were not statistically significant different across the first five days post-emergence (Table 1). On the fifth day post emergence, mosquitoes were more likely to take mixed blood meals (OR = 1.86; 95%CI [1.09–3.19] and p < 0.02); however, it is unclear if this finding has any biological meaning.

Table 1

Mean proportions and Odds ratios of *Ae. aegypti* fed on sugar or blood meals or both meals. Sugar and blood meals were deployed into five cages and the mosquitoes were allowed to access both meals for 24hr, 48hrs,72hrs, 96hrs,120hrs and 144hrs in cage 1,2,3,4 and 5 respectively post emergence.
Days post emergence	N	n	Mean proportion	Odds Ratio	95%CI	p-value
Day1
Blood fed	8	299	0.38	1	-	-
Sugar fed	8	299	0.27	0.59	0.32–1.10	0.10
Mixed fed	8	299	0.28	0.64	0.39–1.05	0.08
Day 2
Blood fed	8	301	0.31	1	-	-
Sugar fed	8	301	0.20	0.56	0.27–1.16	0.12
Mixed fed	8	301	0.34	1.16	0.52–2.58	0.72
Day 3
Blood fed	8	332	0.17	1	-	-
Sugar fed	8	332	0.23	1.46	0.69–3.08	0.32
Mixed	8	332	0.30	2.01	0.90–4.51	0.09
Day 4
Blood fed	8	304	0.20	1	-	-
Sugar fed	8	304	0.22	1.17	0.69–2.00	0.55
Mixed	8	304	0.26	1.44	0.81–2.54	0.22
Day5
Blood fed	8	295	0.18	1	-	-
Sugar fed	8	295	0.26	1.57	0.93–2.67	0.10
Mixed	8	295	0.29	1.86	1.09–3.19	0.02
N = number of replicates; n = total number of released mosquitoes; 95% CI – 95% confidence intervals.

Experiment 2&3 - Aedes aegypti meal choice and the effect of sugar source availability on blood feeding before and after first gonotrophic cycle.

a) Aedes aegypti meal choice before and after first gonotrophic cycle

A significant number of Ae. aegypti preferred to feed on a blood meal over sugar meal within 24 hours before and after first gonotrophic cycle Fig. 3. Out of 385 mosquitoes given meal choice before first gonotrophic cycle, approximately 51.6% (95%CI; 40.2–63.0) preferred to feed on blood only; 9.5% (95%CI; 4.8–14.1) on sugar only and 33.3% (95%CI; 33.4–46.1) on both meals. Moreover, post oviposition 61% (95%CI; 46.9–75.0) fed on blood meal only, 14.6% (95%CI; 5.8–23.4) on sugar only and 6.8% (95%CI; 0.2–13.5) on both meals Fig. 3.

b) Effect of sugar source availability on Aedes aegypti blood feeding preference before and after first gonotrophic cycle.

The results showed that the presence of sugar meal, diverts blood feeding preference on nulliparous and parous Ae. aegypti Table 2. When given both rabbit (blood meal) and sugar meal in the same cage, the number of nulliparous Ae. aegypti that fed on blood only was significantly few (OR = 0.06; 95%CI= [0.02–0.16] and p-value < 0.001) compared to those in a cage that had rabbit only (blood meal only) and was marginally significant on parous mosquitoes (OR = 0.8; 95%CI = 0.57–1.03]; p-value < 0.08) Table 2.

Table 2

Percentage mean and Odds ratios (OR) of blood fed nullparous and parous *Aedes aegypti* given blood meal only or both blood and sugar meal in the same 1m x 1m x1m cage for 24 hours.
Parity status	Meal feeding preference	N	n	%mean fed (95%CI)	OR	95%CIOR	p-value
Nulliparous (Before first gonotrophic cycle)	Blood fed in cage with blood meal only	10	389	99.0(98.0-99.9)	1	-
Nulliparous (Before first gonotrophic cycle)	Blood fed in cage with sugar and blood meal	10	385	85.0(76.5–93.5)	0.06	0.02–0.16	< 0.001
Parous (After first gonotrophic cycle)	Blood fed in cage with blood meal only	10	427	73.3(60.7–85.9)	1	-
Parous (After first gonotrophic cycle)	Blood fed in cage with sugar and blood meal	10	443	67.8(54.8–80.8)	0.8	0.57–1.03	0.08
N = number of replicates; n = total number of released mosquitoes; 95% CI – 95% confidence intervals.

Female Aedes aegypti sugar feeding varies depending on the stage of the life cycle. The present study showed that at nulliparous stage, sugar and blood meals feeding is a parallel and inseparable facet for Ae. aegypti. However, shortly after the completion of the gonotrophic cycle blood meal becomes a major requirement for Ae. aegypti over sugar meal. This is likely to occur as a response to the depleted protein reserves used during gonotrophic cycle window and the need for additional protein for the next gonotrophic cycle. Mosquitoes require energy mainly from sugar sources for survival, fitness and fecundity [1], [4], they do so shortly after emergence. On the other hand they need a protein [3] for eggs development. The highlighted functions indicate that the two meals are components which need to concurrently occur for the existence of the mosquitoes.

Also, the existence of sugar reserves from the sugar meal taken before and during the gonotrophic cycle may be the underlying reason for Ae. aegypti not requiring more energy from another sugar meal after first gonotrophic cycle. This hypothesis concurs with the findings which reported that carbohydrates taken by Ae. aegypti during larval stage and earlier adult stage are usually stored and used during and after gonotrophic cycle [20], [21]. The ability of Ae. aegypti to store carbohydrates for future have may be enabled the mosquitoes to adapt living in areas with low or inadequate sugar sources. And also influenced the anautogenous mosquitoes to predominantly feed on blood[22]. The adaptive restriction to only blood meal increases human contact frequency[23], a behaviour which is described as a fundamental parameter for transmission of vector borne diseases.

Furthermore, this study demonstrated that mixed feeding (sugar and blood meal) was a common practice for Ae. aegypti particularly at nulliparous stage. The concept of mosquitoes feeding on both meals (blood and sugar meals) highlights an important view for developing intervention such as attractive toxic sugar bait (ATSB) against Ae. aegypti, the intervention that is reported to work against other stegomyia mosquitoes such as Aedes albopictus [24]–[26]. In fact, the mixed meal feeding occurred in a controlled environment (semi-field system) using insectary-reared mosquitoes but we don’t know yet if the same behaviour may occur in the wild population if the opportunity to sugar feeding is provided.

The majority of nulliparous and parous Ae. aegypti which were pre-fed on sugar meal preferred to take blood meal over sugar meal when offered a constant choice between the two meals. The hypothesis underlying the observed findings may be that, the mosquitoes had enough sugar reserves which was obtained in the pre-sugar feeding, thus they were no longer in need of energy rather they needed a protein for first and second gonotrophic cycles. Even though, the pre-sugar fed Ae. aegypti prefers blood meal over sugar meal, on other hand a mixed meal intake is favoured at nulliparous stage than parous stage. This implies that, at younger age, Ae. aegypti needs more energy than at old stage. Moreover, when both sugar and blood sources were available, mosquito blood feeding rate was considerable reduced compared to when only blood host was available. The reduction of mosquito blood feeding due to availability of a sugar source has great implications for vector control strategies using intervention such as ATSBs as it proves that it may also reduce blood feeding frequency, which would have major implications for disease transmission and vectoral capacity [27]. Previous studies reported that in the presence of a blood meal Ae. aegypti would exclusively feed on blood [1]. However, this contrasts with the current and other studies which researched for the same mosquito ecological behaviour and found that in some areas Ae. aegypti do feed on sugar[13], [14], implying that the tendency may be attributed by the availability of sugar sources.

On the other hand, this study found that the presence of a blood meal did not alter Ae. aegypti sugar feeding preference, implying that despite that, Ae. aegypti do infrequently feed on sugar [28] but still the phenomenon remains consistent even when the blood source is easily available. The observation, cements the concept that, sugar meal is a part and parcel of mosquito life [1] and blood meal alone is insufficient to fulfil the mosquito energy requirement.

Limitation and safety consideration.

In this study, mosquitoes had to be provided a constant choice between a human (source of blood meal) and a sugar bait (sugar meal) over a couple of days. However, it would be impractical to constantly keep humans in cages for couple days. Thus, rabbit was chosen as alternative host.

Nulliparous and parous Ae. aegypti have ecological difference in responding to sugar and blood meals. While nulliparous Ae. aegypti aging 1–5 days have more less similar affinity to sugar and blood meals, parous Ae. aegypti prefer more a blood meal only over a sugar meal only. Also, sugar meal seems to be a mosquito blood meal questing divergent at the early mosquito stage of life. Therefore, the early sugar feeding behaviour and the divergent property of the sugar against Ae. aegypti may have a significant epidemiological implication through the development of vector control tools such as attractive toxic sugar bait (ATSB) which may target mosquitoes with arboviruses that have not reached the infective stages.

Acknowledgments

The authors would like to thank all staff of Ifakara Health Institute for their support. Also, we would like to extend our heartfelt thanks to Wellcome Trust for funding this study (Grant No. 203291/Z/16/Z).

Funding

This study was funded by Wellcome Trust, 215 Euston Road, London NW1 2BE, UK. A funding body was not involved in any role rather than providing funds to conduct a study.

Availability of data and materials

The datasets generated during the study will be available in a Europe PubMed Central

Ifakara Health Institute saver and corresponding author on reasonable request.

Authors’ contribution

FCT, FOO and MFM designed the experiments. FCT, RKM, ABM and JJM conducted experiments. FCT and MFM analysed data. FCT, JKS and MFM wrote the paper and all other authors reviewed and contributed to the final draft. All authors read and approved the final manuscript draft.

Ethical approval and consent to participate

This study received an ethical approval from Ifakara Health Institute Review Board (IHI-IRB) No. IHI/IRB/No. 22-2017 and National Institute for Medical Research Review Board (NIMR-RB) No. NIMR/HQ/R.8a/Vol. IX/2813. All data were collected by conducting experiments using animals (rabbits) nursed at Ifakara Health Institute-Bagamoyo branch following good laboratory practice procedures and were used according to the Animal Welfare Act (2008) that gives a guiding on protection of animal used in a scientific research.

Consent for publication

Not applicable

Competing interests

The authors declare that they have no competing interests.

Authors’ information

1.Ifakara Health Institute, P.O.Box 74, Bagamoyo, Pwani, United Republic of Tanzania.

2.Kemri Wellcome Trust Research Programme, CGMRC, P.O.Box 230-80108, Kilifi, Kenya.

3.School of Medical Sciences, Fuculty of Biology, Medicine and Health, The University of Manchester, 1.485 Stopford Building, Manchester, M13 9PL.

4.The Nelson Mandela African Institution of Science and Technology: School of life Science and Bio-Engineering, P.O.Box 447 Arusha, Tanzania.

5.Faculty of Health Science, School of Public Health, University of the Witwatersrand, Johannesburg, South Africa.

*Corresponding author

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No competing interests reported.

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Evaluation of Aedes aegypti sugar feeding behaviour in a semi-field system in Tanzania

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Abstract

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Background

Methods

Mosquitoes

Data analysis

Results

a) Aedes aegypti meal choice before and after first gonotrophic cycle

Discussion

Conclusions

Declarations

References

Additional Declarations

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