Heather Ferguson - Academia.edu (original) (raw)

Papers by Heather Ferguson

I Chapter 1: General introduction 4 1.1 Why study parasites?' 4 1.2 Importance of parasites i... more I Chapter 1: General introduction 4 1.1 Why study parasites?' 4 1.2 Importance of parasites in nature 4 1.3 Parasites and evolution 5 1.4 Evolution of virulence 6 1.5 Evolution and epidemiology of vector-borne disease 9 1.6 Malaria: natural history and epidemiology 11 1.6.1 Plasmodium life cycle 12 1.6.2 Anopheles life cycle 13 1.6.3 Epidemiology 13 1.7 Evolution of virulence in malaria 14 1.7.1 Vertebrate host mortality 16 1.7.2 Vertebrate host morbidity 17 1.7.3 Vertebrate host genotype 17 1.7.4 Vector fitness 18 1.8 Experimental system 19 1.8.1 The parasite 20 1.8.2 The vertebrate host 20 1.8.3 The vector 21 1.8.4 Generality of the model system 22 1.9 Thesis aims and overview 24 Chapter 2: What is the general impact of malaria parasites on mosquito survival? 26 2.1 Summary 26 2.2 Introduction 26 2.3 Methods 28 2.4 Results 33 2.4.1 Overall effect 33 2.4.2 Choice of species 35 2.4.3 Length of study 36 2.4.4 Dose effects 37 2.4.5 Environmental conditions 38 2.4.6 Choice of contr...

Oxford Scholarship Online

The term “dilution effect” describes scenarios where pathogen transmission is reduced as host div... more The term “dilution effect” describes scenarios where pathogen transmission is reduced as host diversity increases. Theoretical frameworks exist to predict conditions under which dilution effects may arise, with vector-borne diseases (VBDs) being particularly susceptible to host diversity. However, to date, empirical investigation of dilution effects has been restricted to a few temperate VBD systems. We review the potential contribution of dilution effects for VBDs of greatest public health importance in low-income, typically tropical, countries. Using examples, we discuss how the underlying ecology of pathogen and vector species combine to determine the response of the disease system to biodiversity. We review cases demonstrating how manipulation of host-species diversity has altered human exposure risk. We caution that attempts to control VBDs by manipulating host diversity are unlikely to succeed, and may even be detrimental, without having a detailed understanding of the local e...

Parasites & vectors, Jan 14, 2018

Widespread deforestation occurring in the tropics is hypothesized to impact the transmission of v... more Widespread deforestation occurring in the tropics is hypothesized to impact the transmission of vector-borne diseases (VBD). Predicting how environmental changes will impact VBD transmission is dependent on understanding the ecology and behaviour of potential vector species outside of domestic settings. However there are few reliable sampling tools for measuring the habitat preference and host choice of mosquito vectors; with almost none suitable for sampling recently blood-fed, resting mosquitoes. This study evaluated the use of two mosquito traps: the resting bucket (RB) and sticky resting bucket (SRB) traps relative to CDC backpack aspiration (CDC) for sampling mosquitoes resting in a range of habitats representing a gradient of deforestation. Eight habitats were selected for sampling around two villages in Kudat District, Malaysian Borneo, to reflect the range of habitats available to mosquitoes in and around human dwellings, and nearby forest habitats where reservoir hosts are ...

Scientific reports, Jan 8, 2018

Artificial infection of mosquitoes with the endosymbiont bacteria Wolbachia can interfere with ma... more Artificial infection of mosquitoes with the endosymbiont bacteria Wolbachia can interfere with malaria parasite development. Therefore, the release of Wolbachia-infected mosquitoes has been proposed as a malaria control strategy. However, Wolbachia effects on vector competence are only partly understood, as indicated by inconsistent effects on malaria infection reported under laboratory conditions. Studies of naturally-occurring Wolbachia infections in wild vector populations could be useful to identify the ecological and evolutionary conditions under which these endosymbionts can block malaria transmission. Here we demonstrate the occurrence of natural Wolbachia infections in three species of black fly (genus Simulium), which is a main vector of the avian malaria parasite Leucocytozoon. Prevalence of Leucocytozoon was high (25%), but the nature and magnitude of its association with Wolbachia differed between black fly species. Wolbachia infection was positively associated with avia...

Wellcome open research, 2017

Mosquito behaviours including the degree to which they bite Background inside houses or outside i... more Mosquito behaviours including the degree to which they bite Background inside houses or outside is a crucial determinant of human exposure to malaria. Whilst seasonality in mosquito vector abundance is well documented, much less is known about the impact of climate on mosquito behaviour. We investigated how variations in household microclimate affect outdoor-biting by malaria vectors, and. Anopheles arabiensis Anopheles funestus : Mosquitoes were sampled indoors and outdoors weekly using Methods human landing catches at eight households in four villages in southeastern Tanzania, resulting in 616 trap-nights over 12 months. Daily temperature, relative humidity and rainfall were recorded. Generalized additive mixed models (GAMMs) were used to test associations between mosquito abundance and the microclimatic conditions. Generalized linear mixed models (GLMMs) were used to investigate the influence of microclimatic conditions on the tendency of vectors to bite outdoors (proportion of outdoor biting). : abundance peaked during high rainfall months Results An. arabiensis (February-May), whilst density remained stable into the dry An. funestus season (May-August) Across the range of observed household temperatures,. a rise of 1 C marginally increased nightly abundance (~11%), An. arabiensis but more prominently increased abundance (~66%). The An. funestus abundance of and showed strong positive An. arabiensis An. funestus associations with time-lagged rainfall (2-3 and 3-4 weeks before sampling). The degree of outdoor biting in was significantly associated with the An. arabiensis relative temperature difference between indoor and outdoor environments, with exophily increasing as temperature inside houses became relatively warmer. The exophily of did not vary with temperature differences. An. funestus : This study demonstrates that malaria vector shifts Conclusions An. arabiensis the location of its biting from indoors to outdoors in association with relative differences in microclimatic conditions. These environmental impacts could give rise to seasonal variation in mosquito biting behaviour and degree of protection provided by indoor-based vector control strategies.

Parasites & vectors, Jan 18, 2017

Plasmodium knowlesi is found in macaques and is the only major zoonotic malaria to affect humans.... more Plasmodium knowlesi is found in macaques and is the only major zoonotic malaria to affect humans. Transmission of P. knowlesi between people and macaques depends on the host species preferences and feeding behavior of mosquito vectors. However, these behaviours are difficult to measure due to the lack of standardized methods for sampling potential vectors attracted to different host species. This study evaluated electrocuting net traps as a safe, standardised method for sampling P. knowlesi vectors attracted to human and macaque hosts. Field experiments were conducted within a major focus on P. knowlesi transmission in Malaysian Borneo to compare the performance of human (HENET) or macaque (MENET) odour-baited electrocuting nets, human landing catches (HLC) and monkey-baited traps (MBT) for sampling mosquitoes. The abundance and diversity of Anopheles sampled by different methods were compared over 40 nights, with a focus on the P. knowlesi vector Anopheles balabancensis. HLC caught...

Parasitology, Jan 27, 2017

Plasmodium knowlesi is increasingly recognized as a major cause of malaria in Southeast Asia. Ano... more Plasmodium knowlesi is increasingly recognized as a major cause of malaria in Southeast Asia. Anopheles leucosphyrous group mosquitoes transmit the parasite and natural hosts include long-tailed and pig-tailed macaques. Despite early laboratory experiments demonstrating successful passage of infection between humans, the true role that humans play in P. knowlesi epidemiology remains unclear. The threat posed by its introduction into immunologically naïve populations is unknown despite being a public health priority for this region. A two-host species mathematical model was constructed to analyse this threat. Global sensitivity analysis using Monte Carlo methods highlighted the biological processes of greatest influence to transmission. These included parameters known to be influential in classic mosquito-borne disease models (e.g. vector longevity); however, interesting ecological components that are specific to this system were also highlighted: while local vectors likely have intr...

Scientific reports, Jan 17, 2017

The efficiency of malaria parasite development within mosquito vectors (sporogony) is a critical ... more The efficiency of malaria parasite development within mosquito vectors (sporogony) is a critical determinant of transmission. Sporogony is thought to be controlled by environmental conditions and mosquito/parasite genetic factors, with minimal contribution from mosquito behaviour during the period of parasite development. We tested this assumption by investigating whether successful sporogony of Plasmodium falciparum parasites through to human-infectious transmission stages is influenced by the host species upon which infected mosquitoes feed. Studies were conducted on two major African vector species that generally are found to differ in their innate host preferences: Anopheles arabiensis and An. gambiae sensu stricto. We show that the proportion of vectors developing transmissible infections (sporozoites) was influenced by the source of host blood consumed during sporogony. The direction of this effect was associated with the innate host preference of vectors: higher sporozoite pr...

Malaria journal, Jan 15, 2016

PLOS Neglected Tropical Diseases, 2016

Background In recent years, the primate malaria Plasmodium knowlesi has emerged in human populati... more Background In recent years, the primate malaria Plasmodium knowlesi has emerged in human populations throughout South East Asia, with the largest hotspot being in Sabah, Malaysian Borneo. Control efforts are hindered by limited knowledge of where and when people get exposed to mosquito vectors. It is assumed that exposure occurs primarily when people are working in forest areas, but the role of other potential exposure routes (including domestic or peri-domestic transmission) has not been thoroughly investigated. Methodology/Principal Findings We integrated entomological surveillance within a comprehensive case-control study occurring within a large hotspot of transmission in Sabah, Malaysia. Mosquitoes were collected at 28 pairs households composed of one where an occupant had a confirmed P. knowlesi infection within the preceding 3 weeks ("case") and an associated "control" where no infection was reported. Human landing catches were conducted to measure the number and diversity of mosquitoes host seeking inside houses and in the surrounding peri-domestic (outdoors but around the household) areas. The predominant malaria vector species was Anopheles balabacensis, most of which were caught outdoors in the early evening (6pm-9pm). It was significantly more abundant in the peri-domestic area than inside houses (5.5-fold), and also higher at case than control households (0.28±0.194 vs 0.17 ±0.127, p<0.001). Ten out of 641 An. balabacensis tested were positive for simian malaria parasites, but none for P. knowlesi.

PLoS genetics, Sep 1, 2016

Malaria transmission is dependent on the propensity of Anopheles mosquitoes to bite humans (anthr... more Malaria transmission is dependent on the propensity of Anopheles mosquitoes to bite humans (anthropophily) instead of other dead end hosts. Recent increases in the usage of Long Lasting Insecticide Treated Nets (LLINs) in Africa have been associated with reductions in highly anthropophilic and endophilic vectors such as Anopheles gambiae s.s., leaving species with a broader host range, such as Anopheles arabiensis, as the most prominent remaining source of transmission in many settings. An. arabiensis appears to be more of a generalist in terms of its host choice and resting behavior, which may be due to phenotypic plasticity and/or segregating allelic variation. To investigate the genetic basis of host choice and resting behavior in An. arabiensis we sequenced the genomes of 23 human-fed and 25 cattle-fed mosquitoes collected both in-doors and out-doors in the Kilombero Valley, Tanzania. We identified a total of 4,820,851 SNPs, which were used to conduct the first genome-wide estim...

Proceedings of the National Academy of Sciences of the United States of America, Aug 9, 2016

Malaria transmission has been substantially reduced across Africa through the distribution of lon... more Malaria transmission has been substantially reduced across Africa through the distribution of long-lasting insecticidal nets (LLINs). However, the emergence of insecticide resistance within mosquito vectors risks jeopardizing the future efficacy of this control strategy. The severity of this threat is uncertain because the consequences of resistance for mosquito fitness are poorly understood: while resistant mosquitoes are no longer immediately killed upon contact with LLINs, their transmission potential may be curtailed because of longer-term fitness costs that persist beyond the first 24 h after exposure. Here, we used a Bayesian state-space model to quantify the immediate (within 24 h of exposure) and delayed (>24 h after exposure) impact of insecticides on daily survival and malaria transmission potential of moderately and highly resistant laboratory populations of the major African malaria vector Anopheles gambiae Contact with LLINs reduced the immediate survival of moderate...

Malaria Journal, 2016

Background: Reliable quantification of mosquito host-seeking behaviours is required to determine ... more Background: Reliable quantification of mosquito host-seeking behaviours is required to determine the efficacy of vector control methods. For malaria, the gold standard approach remains the risky human landing catch (HLC). Here compare the performance of an improved prototype of the mosquito electrocuting grid trap (MET) as a safer alternative with HLC for measuring malaria vector behaviour in Dar es Salaam, Tanzania. Methods: Mosquito trapping was conducted at three sites within Dar es Salaam representing a range of urbanicity over a 7-month period (December 2012-July 2013, 168 sampling nights). At each site, sampling was conducted in a block of four houses, with two houses being allocated to HLC and the other to MET on each night of study. Sampling was conducted both indoors and outdoors (from 19:00 to 06:00 each night) at all houses, with trapping method (HLC and MET) being exchanged between pairs of houses at each site using a crossover design. Results: The MET caught significantly more Anopheles gambiae sensu lato than the HLC, both indoors (RR [95 % confidence interval (CI)]) = 1.47 [1.23-1.76], P < 0.0001 and outdoors = 1.38 [1.14-1.67], P < 0.0001). The sensitivity of MET compared with HLC did not detectably change over the course of night for either An. gambiae s.l. (OR [CI]) = 1.01 [0.94-1.02], P = 0.27) or Culex spp. (OR [CI]) = 0.99 [0.99-1.0], P = 0.17) indoors and declined only slightly outdoors: An. gambiae s.l. (OR [CI]) = 0.92 [0.86-0.99], P = 0.04), and Culex spp. (OR [CI]) = 0.99 [0.98-0.99], P = 0.03). MET-based estimates of the proportions of mosquitoes caught indoors (P i) or during sleeping hours (P fl), as well as the proportion of human exposure to bites that would otherwise occurs indoors (π i), were statistically indistinguishable from those based on HLC for An. gambiae s.l. (P = 0.43, 0.07 and 0.48, respectively) and Culex spp. (P = 0.76, 0.24 and 0.55, respectively). Conclusions: This improved MET prototype is highly sensitive tool that accurately quantifies epidemiologically-relevant metrics of mosquito biting densities, behaviours and human exposure distribution.

Canadian Journal of Zoology, Jul 1, 2000

Dicamptodon tenebrosus is a species at risk in Canada and little is known about its ability to re... more Dicamptodon tenebrosus is a species at risk in Canada and little is known about its ability to recover from disturbance at any scale. I tested whether stream-dwelling larvae are capable of recolonising regions subjected to small disturbances (25-to 40-m artificially depleted reaches) within 1 year, and compared the contributions of larval dispersal and adult reproduction to repopulation of barren areas. Numerical recovery from depletions in these stream sections was predicted to take 6-42 months. Only 4-5% of larvae in reaches adjacent to the depleted zones became colonists in 13 months. Colonisation occurred both by upstream and downstream movements and by larvae of different sizes. Local reproduction appears to be a more effective means of repopulating an area than larval immigration. In one reproductive event, an adult female could provide an equal or greater number of colonists than is supplied by neighbouring stream sections holding 200+ larvae. Résumé : Dicamptodon tenebrosus est une espèce à risque au Canada et l'on ne connaît pas son aptitude à se remettre d'une perturbation de quelque ordre que ce soit. J'ai tenté de déterminer si les larves d'un ruisseau sont capables de recoloniser des zones de perturbations légères (25-40 m de sections appauvries artificiellement) en moins de 1 an et j'ai comparé la repopulation des zones évacuées attribuable à la dispersion larvaire et celle attribuable à la reproduction des adultes. Nous avons prédit que la récupération numérique dans les zones appauvries prendrait de 6 à 42 mois. Seulement 4-15 % des larves dans les zones adjacentes aux zones appauvries ont recolonisé ces zones après 13 mois. La colonisation s'est faite par des déplacements vers l'amont et vers l'aval de larves de différentes tailles. La reproduction locale semble être une méthode de recolonisation plus efficace que l'immigration larvaire. Au cours d'un épisode de reproduction, une femelle adulte a pu produire un nombre égal ou plus grand de colonisateurs que des sections avoisinantes de ruisseau contenant 200+ larves.

PLOS Medicine, 2016

Surveillance is critical to manage preventative health services and control infectious diseases. ... more Surveillance is critical to manage preventative health services and control infectious diseases. Integrated surveillance involving public health, veterinary, and environmental sectors is urgently needed to effectively manage zoonoses and vector-borne diseases. However, most surveillance in low-income countries is paper-based, provides negligible timely feedback, is poorly incentivised, and results in delays, limited reporting, inaccurate data, and costly processing. • The potential of mobile technologies for improving health system surveillance has been demonstrated through small-scale pilots, but large-scale evaluations under programmatic implementation remain rare.

PLOS Neglected Tropical Diseases, 2015

Background The simian malaria parasite Plasmodium knowlesi is emerging as a public health problem... more Background The simian malaria parasite Plasmodium knowlesi is emerging as a public health problem in Southeast Asia, particularly in Malaysian Borneo where it now accounts for the greatest burden of malaria cases and deaths. Control is hindered by limited understanding of the ecology of potential vector species. Methodology/Principal Findings We conducted a one year longitudinal study of P. knowlesi vectors in three sites within an endemic area of Sabah, Malaysia. All mosquitoes were captured using human landing catch. Anopheles mosquitoes were dissected to determine, oocyst, sporozoites and parous rate. Anopheles balabacensis is confirmed as the primary vector of. P. knowlesi (using nested PCR) in Sabah for the first time. Vector densities were significantly higher and more seasonally variable in the village than forest or small scale farming site. However An. balabacensis survival and P. knowlesi infection rates were highest in forest and small scale farm sites. Anopheles balabacensis mostly bites humans outdoors in the early evening between 1800 to 2000hrs. Conclusions/Significance This study indicates transmission is unlikely to be prevented by bednets. This combined with its high vectorial capacity poses a threat to malaria elimination programmes within the region.

Methods in ecology and evolution / British Ecological Society, 2015

1. 'Will my study answer my research question?' is the most fundamental question a researcher can... more 1. 'Will my study answer my research question?' is the most fundamental question a researcher can ask when designing a study, yet when phrased in statistical terms-'What is the power of my study?' or 'How precise will my parameter estimate be?'few researchers in ecology and evolution (EE) try to answer it, despite the detrimental consequences of performing under-or overpowered research. We suggest that this reluctance is due in large part to the unsuitability of simple methods of power analysis (broadly defined as any attempt to quantify prospectively the 'informativeness' of a study) for the complex models commonly used in EE research. With the aim of encouraging the use of power analysis, we present simulation from generalized linear mixed models (GLMMs) as a flexible and accessible approach to power analysis that can account for random effects, overdispersion and diverse response distributions. 2. We illustrate the benefits of simulation-based power analysis in two research scenarios: estimating the precision of a survey to estimate tick burdens on grouse chicks and estimating the power of a trial to compare the efficacy of insecticide-treated nets in malaria mosquito control. We provide a freely available R function, sim.glmm, for simulating from GLMMs. 3. Analysis of simulated data revealed that the effects of accounting for realistic levels of random effects and overdispersion on power and precision estimates were substantial, with correspondingly severe implications for study design in the form of up to fivefold increases in sampling effort. We also show the utility of simulations for identifying scenarios where GLMM-fitting methods can perform poorly. 4. These results illustrate the inadequacy of standard analytical power analysis methods and the flexibility of simulation-based power analysis for GLMMs. The wider use of these methods should contribute to improving the quality of study design in EE.

Malaria journal, Jan 27, 2006

Release of genetically-modified (GM) or sterile male mosquitoes for malaria control is hampered b... more Release of genetically-modified (GM) or sterile male mosquitoes for malaria control is hampered by inability to assess the age and mating history of free-living male Anopheles. Age and mating-related changes in the reproductive system of male Anopheles gambiae were quantified and used to fit predictive statistical models. These models, based on numbers of spermatocysts, relative size of sperm reservoir and presence/absence of a clear area around the accessory gland, were evaluated using an independent sample of mosquitoes whose status was blinded during the experiment. The number of spermatocysts in male testes decreased with age, and the relative size of their sperm reservoir increased. The presence of a clear area around accessory glands was also linked to age and mating status. A quantitative model was able to categorize males from the blind trial into age groups of young (< or = 4 days) and old (> 4 days) with an overall efficiency of 89%. Using the parameters of this mode...