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Knowledge for a sustainable world

Professor Gabriella Gibson

BA, DPhil, Fellow of the Royal Entomological Society
Biography

Gabriella Gibson obtained her PhD on Mosquito Behaviour at the University of Sussex (1978-81), in the laboratory of Dr Mick Gillies (field entomologist) and Dr Mike Jones (circadian rhythms physiologist) and collaborated with colleagues in the Centre for Excellence in Neurophysiology, specialising in visually controlled behaviour in nocturnal mosquitoes.

Her first Post-doc research position was at Imperial College at the Silwood Park site (1981- 1986), supervised by Dr John Brady, an expert in the circadian control of behaviour in tsetse fly, where she extended her techniques in video-recording of flight behaviour in laboratory to field studies in Zimbabwe. She demonstrated that tsetse do not ‘see’ zebras, and therefore, rarely feed on them, and that tsetse use a novel mechanism for using host odours to locate favoured hosts. Over the course of four field season she also witnessed the development of the famous tsetse traps and targets developed by Vale, Hargrove, Torr, Hall and others, which has become the iconic case-study that shows basic principles of sensory control of behaviour are key to the design of successful surveillance and control devices

She then took up a Lectureship at the London School of Hygiene and Tropical Medicine (1987-1991), where she began her long-term ambition to apply the principles of behaviour and the tools she had acquired this far to the study and control of mosquitoes; e.g., analysis of the limits of nocturnal vision, characterisation of the anatomy of mosquito eyes and development of a novel, behaviourally sensitive bioassay to measure the efficacy of insecticides, which has since been adopted by the WHO.

A return to Imperial College at Silwood Park (1992-1998) led to collaborations with Prof. Mario Coluzzii and his protégé Dr Carlo Costantini, with further laboratory and field studies of the host-seeking behaviour of malarial mosquitoes, which led to the development of the first odour-baited entry trap for malarial mosquitoes and a greater understanding of the significant role CO2 plays in relation to the background of many other host odours.

Gibson joined NRI in 1998, where she has pursued her interest in identifying sensory-controlled behaviours in malarial mosquitoes that can be exploited to monitor and control a wide range of disease vectors.

Key research findings:

  • Fieldwork in Zimbabwe demonstrated tsetse alter their flight course to maintain contact with animal odour plumes.
  • The fieldwork also showed the visual-ecology of tsetse eyes is well-matched to the time of day they are active, their flight speed and visual features of the landscape.
  • A zebra's stripes make it all but invisible to tsetse.
  • Integrated vector control can protect cattle-owning pastoralists in sub-Sahara Africa from tsetse affecting cattle health and mosquitoes affecting human health, based on field work in Ethiopia.
  • The eyes of nocturnal mosquitoes have evolved previously unknown mechanisms to heighten their sensitivity to light, which enables them to control flight using only starlight,
  • Mosquitoes communicate through the sounds produced by their wing-beats during swarming and mating interactions
  • Key differences in swarming behaviour and sound communication between closely related mosquito species help explain apparent reproductive isolation and ultimately speciation in the malarial mosquito Anopheles gambiae species complex, with fieldwork in Burkina Faso.

Gibson's current key external collaborators include Prof. I.J. Russell (University of Brighton), Prof. S.J. Torr (Liverpool School of Tropical Medicine), Dr R. Dabiré (Institute of Malarial Research, Burkina Faso) and Dr Rousseau Djouaka (IITA, Benin) Dr Jolyon Medlock & Alex Vaux (PHE).

The main aim of Professor Gibson's research is to elucidate how disease-transmitting insects use their sensory systems (vision, hearing, smell, taste and touch) to obtain the information they need from the outside world to guide the behaviours that are essential for their survival; e.g. locating a suitable mate, finding their blood-hosts and locating a suitable place to lay their eggs.

Her research is inter-disciplinary, involving the study of animal behaviour, sensory physiology and neurophysiology. Fieldwork is crucial to establish the context in which behaviours occur, and laboratory studies are required to investigate the details of sensory-guided behaviour where the most essential environmental parameters can be recreated and manipulated by the experimenter. The aim is to identify key stimuli that guide behaviour and how those stimuli are used by the sensory-motor systems of insects. Knowledge of behaviour is a prerequisite to the development of well-designed tools to monitor and control pest insects and contributes insights into how sensory systems work in higher order animals.

Professor Gibson's research is based at the NRI in laboratories instrumented with 3D video and sound recording facilities and in the field, currently in Burkina Faso, West Africa. Her published work has contributed to understanding of how specific aspects of tsetse and mosquito vision and olfaction help them to find blood-hosts, designed an improved, standardised trap for malarial mosquito species and a more sensitive bioassay to test new insecticides and discovered a previously unknown mechanism of species-recognition in mosquitoes.

Human Decoy Trap; operational and social acceptability of a novel tool to improve surveillance and control of mosquitoes and other disease
MRC £580k, 2 yrs 2017-19, Role:PI, Collaborators IRSS Burkina Faso and IITA Benin.

Malaria infects over 200 million people every, mostly in sub-Saharan Africa. The malaria parasite is spread by infected mosquitoes and the most effective way to monitor the disease is to monitor populations of these mosquitoes. However, current tools for sampling malarial mosquitoes are time-consuming and labour intensive, making them expensive and difficult to standardize.

We have developed a mosquito trap that exploits the blood-seeking behaviour of mosquitoes by mimicking the sensory stimuli that a mosquito follows when searching for a person to bite. These include the look, smell and temperature of warm-blooded hosts. We have incorporated these stimuli into a trap that lures mosquitoes towards it and then captures them when they land.

We will test this "Human Decoy" Trap against current methods used in mosquito monitoring to determine whether it can overcome the limitations of existing tools. Fieldwork will be conducted in Burkina Faso, Benin and Cameroon, three West African countries where malaria causes thousands of deaths every year, but differing in intensity and seasonality of transmission and with different mosquito species involved to assess potential differences in trap performance in a wide range of malaria settings. We will also work with end-users of the trap (local communities, public health operatives and field technicians) to determine their perspectives and needs regarding mosquito sampling and control. The long-term aim is to develop a commercial prototype that is effective and acceptable to end-users, maximising the likelihood the trap will be adopted into the communities and sectors that need it the most.

The Human Decoy Trap may be deployed as a mosquito control tool by reducing the number of infective mosquito bites a person receives. This is currently achieved by providing people with insecticide-treated bed nets to protect them from bites whilst they sleep and spraying the walls inside houses thus killing mosquitoes that rest there. However, neither of these options protects people from mosquitoes that may bite them outdoors during the day or just before they go to bed at night. The trap may also be effective against other vector species that transmit infectious diseases, such as dengue fever, chikungunya and Zika viruses.

Taking The Bite Out Of Wetlands: Managing Mosquitoes and The Socio-Ecological Value of Wetlands For Wellbeing
NERC £3 m, 3 yrs, 2016-2019, Role Co-I, 4 collaborating Universities.

Interest in the health and wellbeing impacts of wetlands has increased in the UK, in the context of both short and long term responses to extreme weather events and climate change. This is reflected in the UK Wetland Vision (Hume, 2008) that identifies a need to 'make wetlands more relevant to people's lives by better understanding and harnessing the benefits provided by naturally-functioning rivers and wetlands'. Expansion of wetlands can bring many benefits but it can also increase potential for mosquito-borne disease. There is a lack of knowledge about the consequences of wetland expansion for disease risk. This knowledge gap opens up space for speculation in the press and media about the perceived problems of 'killer' mosquitoes spreading across England, which can in turn fuel community unease and opposition to wetland creation and expansion. A key concern of the project is, therefore, to develop ecological interventions and guidance for diverse end-users to minimise mosquito-related problems, framed within and facilitated by a broader understanding of wetland value as impacted by mosquitoes. The potential contribution of wetland development to social and economic wellbeing envisaged in the UK Wetland Vision could be severely constrained by a failure to adequately address the risks imposed by mosquitoes and biting insects.

The overall aim of this project will be to show how positive socio-cultural and ecological values of wetlands can be maximised for wellbeing and negative attitudes reduced. Management interventions for use by Public Health England and general guidelines will be developed to limit the damaging effects of mosquito populations and enhance appreciation of the ecological value of mosquitoes in wetland ecosystems. The project will result in an increase in our understanding of wetland environments and demonstrate how ecological interventions embedded in a broader understanding of wetland valuation can deliver wellbeing benefits to a broad range of stakeholders.

There are four main objectives:

  1. Development of a new conceptual place-based ecosystem services and wellbeing framework for understanding the impact of interventions and wetland values.
  2. Exploration of the value of wetlands and mosquitoes in twelve case study locations.
  3. Production of guidelines for valuing wetlands and managing mosquito populations to enhance the value of British wetlands for wellbeing.
  4. Production of a place-based narrative on the socio-cultural, economic and ecological value of wetlands in British Society in the early years of the 21st Century.

Exploiting acoustic distortion by mosquitoes to listen on the wing. The Leverhulme Trust: £194,000. 2012–14. Role: Co-PI. Collaboration with Prof. I.J. Russell, University of Brighton.

The underlying mechanism of flight tone convergence (see The Wellcome Trust funded project, above) is not well understood. We know that it occurs, remarkably, at frequencies too high for males or females of a given species to hear. The physiological mechanism by which mosquitoes detect and respond differentially to the flight tones of closely related taxa is the subject of this project. It has been shown that mosquito hearing is the most sensitive of all arthropods. Moreover, they can detect and process the sound of another mosquito that is only a few centimetres away, against the background sound of their own flight tones, with both sources of sound simultaneously impinging on the flagella of their antennae. In itself, this acoustic capability is extraordinary and presents valuable insights into the wide variety of hearing mechanisms that have evolved to enhance the sensitivity and specificity of sound detection in insects.

Areas for future research: The ultimate objective is to elucidate the mechanisms by which ecological speciation occurs in the malarial mosquito species complex Anopheles gambiae s.l. at the physiological level. Clearly, when two entities no longer recognise each other as conspecifics, the speciation process is more-or-less complete. The immediate aim of this phase of the project will be to determine the acoustic cues used by An. gambiae M and S forms to distinguish themselves from each other.

The effect of radiation on the mating songs and courtship behaviour of the IAEA colony mosquitoes. Funded by the International Atomic Energy Agency's (IAEA) project on the biology of male mosquitoes in relation to genetic control programmes: £10,000. 2012–13. Role: Chief Scientific Investigator.

The efficacy of the sterile insect technique to control mosquitoes depends to a large extent on the mating competitiveness of released males compared to wild males of the target species. This project successfully demonstrated that male courtship behaviour, especially mate recognition through flight tone harmonisation, is not affected by the colonisation or irradiation of the IAEA colony males.

Areas for future research: This research project established a 'proof of concept' that 'pure' research on mosquito communication has an immediate practical application to the development of novel tools for controlling mosquitoes of public health importance. The current rise in interest in genetically modified or manipulated mosquitoes to control wild mosquito populations provides a welcome opportunity for collaboration. NRI could become a centre of expertise for testing the mating compatibility of engineered and wild strains of target mosquito populations.

A novel acoustic signalling system discovered in mosquitoes: exploring the biophysical and neurophysiological basis for interactive behaviour in an insect. BBSRC: £587,000. 2008–11. Role: Co-PI. Collaborator Prof. I.J. Russell, FRS, University of Sussex and Dr R. Dabiré, IRSS, Burkina Faso.

It has been known for more than 150 years that males use their highly sensitive hearing organ (antennae and Johnston's organ) to locate potential mates by detecting the sound of a con-specific female's wing-beats. In 2006, Professor Gibson and Professor Russell (University of Brighton) discovered that females also detect males, but respond by 'singing a duet' with the male, each one subtly altering the frequency of their wing-beats to converge on a shared harmonic if they are a 'good match'. All-the-while, the male closes in on the female in a high-speed chase.

Remarkably and perhaps uniquely in the insect kingdom, this system of sexual recognition between mosquitoes is based on interactive auditory exchanges between mosquitoes, consisting of continuous changes in wing-beat frequency in response to the detection of simultaneous changes in the wing-beat frequency of the other, unlike the highly stereotypical 'call-response' song patterns of communication described for other insects. This project characterised the behavioural, neurophysiological and biophysical mechanisms of auditory sexual recognition in mosquitoes, which led to our next novel discovery, that the Johnston's organ of mosquitoes is tuned not to the actual wing-beat frequency of the opposite sex, but to different tones in the harmonics of antennal vibrations which are generated by the combined input of flight tones from both mosquitoes. This acoustic distortion has been known to exist in the hearing organs of a range of organisms, but previously described as an interesting epiphenomenon, with no obvious purpose. Mosquitoes, however, appear to use distortion products as sensory cues that enable male–female pairs to communicate through auditory interactions between them. (See: Gibson & Russell, 2006; Warren et al., 2009).

Areas for future research: These results led the researchers to a second phase of research investigating the potential for frequency matching to be used as a mechanism for species recognition, and found that the incipient species Anopheles gambiae s.s. and An. coluzzii from Burkina Faso, where they are sympatric, do not frequency match unless they are paired with their own species (Pennetier et al., 2010; Gibson et al., 2010), and this is the subject of a new project (see The Leverhulme Trust funded project, below).

Research and teaching Lead Pest Behaviour Research Group

  • Chief Medical Editor, Medical and Veterinary Entomology, a journal of the Royal Entomological Society (2004–10)
  • Member of editorial board, Medical and Veterinary Entomology (2002 to present)
  • Molecular Entomology Steering Committee, UNDP/World Bank/WHO Special Programme for Research and Training in Tropical Diseases (TDR) (1999-2006)
  • Member, Association for the Study of Animal Behaviour
  • Member, Brain Research Association
  • Member, American Society of Tropical Medicine & Hygiene
  • Member, Entomological Society of America.

ORCID

https://orcid.org/0000-0002-3127-8027

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