Search bioRxiv⌕ Search

Biology subjects

Cunningham, A. A.

Publications and source records attributed to Cunningham, A. A..

7 recordsLinked to original sources

Repeated and widespread introduction of a mosquito-borne virus, but wildlife impact remains localised in urban area

Mosquito-borne viruses are emerging in new regions with increasing regularity. Shifting climatic envelopes, especially in temperate regions, and altered enzootic cycles are changing likelihoods of persistence, meaning new approaches are required to predict and monitor establishment. Usutu virus (USUV) is a mosquito-borne viral zoonosis, which was first recorded in the United Kingdom in wild birds and mosquitoes in 2020. By developing a multidisciplinary approach, incorporating enhanced passive and active surveillance of wild birds, we discovered previously unrecorded introductions and identified USUV persistence and geographic expansion. By combining molecular and serological testing with citizen science derived datasets, we show an associated marked decline in a common, widespread, and highly susceptible host species (Eurasian Blackbird, Turdus merula). However, the clearest continuous signal of host population decline remains localised to a large urban area, despite the much wider virus distribution. This may be a consequence of an urban heat island effect and associated increase in length of the mosquito active season. Our results indicate that the establishment and impact of future mosquito-borne pathogens in temperate zones, anticipated under climate change, may first be most apparent in urban areas. Consequently, enhanced surveillance efforts in urban areas could provide an efficient mechanism for detecting novel pathogen emergence. The epidemiology of emerging vector-borne diseases, especially in temperate areas, depends on the interplay between climate, land-use and available hosts; therefore, considering each in isolation will not be sufficient to reliably inform surveillance or response planning.

ecology↗

Detection of West Nile Virus via Retrospective Mosquito Arbovirus Surveillance in the United Kingdom

In March 2025, as part of on-going enhanced surveillance for mosquito-borne Orthoflaviviruses, West Nile virus (WNV) RNA was detected in two pools of female Aedes vexans collected in July 2023 in Nottinghamshire, England. Viral RNA detection was achieved via reverse transcription-qPCR. Sequencing and subsequent phylogenetic analysis of a 402 bp fragment indicated that the detections clustered with WNV lineage 1a. The exact origin of this virus remains unclear, but this finding indicates a historic WNV presence in the United Kingdom (UK). Surveillance has not provided evidence of further viral transmission to date.

molecular biology↗

Transovarial transmission in field caught mosquitoes identifies a mechanism for the establishment of Usutu virus in a temperate country

Usutu virus (USUV) is an emerging zoonotic flavivirus in Europe, and the first zoonotic mosquito-borne virus to be confirmed in animal hosts in the United Kingdom (UK). Phylogenetic analysis of USUV in the three years following its initial detection in 2020 indicated that the virus is overwintering in the UK. In 2023, USUV was identified outside Greater London for the first time. Therefore, USUV should now be considered endemic within southeast England. Surveillance of avian hosts and mosquito vectors has been insufficient to elucidate the mechanism by which USUV has persisted through temperate winters. It is likely that mosquitoes play a significant role in facilitating the establishment of USUV in temperate areas, as is the case for related mosquito-borne viruses. Here we undertake enhanced targeted vector surveillance at the index site to investigate the role of mosquitoes in facilitating USUV establishment in the UK. Between 2021 and 2024 inclusive, we detected USUV in host-seeking adult female Culex pipiens s.l. (n = 8/554 pools), a key vector of the virus in Europe. During 2023, enhanced surveillance detected transovarial transmission of USUV in wild Cx. pipiens s.l. (n = 1/202 pools), by screening adults following captive rearing of mosquito larvae collected from the field. This is, to our knowledge, the first description of vertical transmission of USUV in an arthropod vector. Consequently, transovarial transmission should be considered a viable mechanism for the persistence of USUV in temperate areas. Our results highlight the importance of undertaking detailed vector surveillance, across life stages, to inform the epidemiology of vector-borne viruses.

microbiology↗

A series of terribly unfortunate events: How environment and infection synergized to cause the Kihansi spray toad extinction

Outbreaks of emerging infectious diseases are trained by local biotic and abiotic factors, with host declines occurring when conditions favour the pathogen. Extinction of the Tanzanian Kihansi spray toad (Nectophrynoides asperginis) in 2004 was contemporaneous with the construction of a dam, implicating habitat modification in the loss of this species. However, high burdens of a globally emerging infection, Batrachochytrium dendrobatidis (Bd) were synchronously observed implicating infectious disease in this toads extinction. Here, by shotgun sequencing skin DNA from archived toad mortalities and assembling chytrid mitogenomes, we prove this outbreak was caused by the BdCAPE lineage and not the panzootic lineage BdGPL that is widely associated with global amphibian extinctions. Molecular dating showed an invasion of BdCAPE across Southern Africa overlapping with the timing of the extinction event. However, post-outbreak surveillance of conspecific species inhabiting this mountainous region showed widespread infection by BdCAPE yet no signs of amphibian ill-health or species decline. Our findings show that despite efforts to mitigate the environmental impact caused by dams construction, invasion of the pathogen ultimately led to the loss of the Kihansi spray toad; a synergism between emerging infectious disease and environmental change that likely heralds wider negative impacts on biodiversity in the Anthropocene.

ecology↗

Manipulating vector transmission reveals local processes in bacterial communities of bats

Infectious diseases result from multiple interactions among microbes and hosts, but community ecology approaches are rarely applied. Manipulation of vector populations provides a unique opportunity to test the importance of vectors in infection cycles while also observing changes in pathogen community diversity and species interactions. Yet for many vector-borne infections in wildlife, a biological vector has not been experimentally verified and few manipulative studies have been performed. Using a captive colony of fruit bats in Ghana, we observed changes in the community of Bartonella bacteria over time after the decline and subsequent reintroduction of bat flies. With reduced transmission, community changes were attributed to ecological drift and potential selection through interspecies competition mediated by host immunity. This work demonstrated that forces maintaining diversity in communities of free-living macroorganisms act in similar ways in communities of symbiotic microorganisms, both within and among hosts. Additionally, this study is the first to experimentally test the role of bat flies as vectors of Bartonella species.

ecology↗

Disease driven extinction in the wild of the Kihansi spray toad (Nectophrynoides asperginis)

The Kihansi spray toad, Nectophrynoides asperginis, became extinct in the wild despite population monitoring and conservation management of its habitat in the Kihansi gorge, Tanzania. Anecdotal evidence has indicated human induced habitat modification, predators, pesticides and disease as possible causes of a rapid population decline and the species extirpation. Here, we systematically investigate the role of disease in the extinction event of the wild toad population. The amphibian chytrid fungus, Batrachochytrium dendrobatidis, was detected in spray toads that died during the extinction event and subsequently in other amphibian species in Kihansi Gorge and the adjacent Udagaji Gorge, but not in any toads collected prior to this. Following the population decline, the remnant spray toad population gradually disappeared over a nine-month period. We demonstrate how demographic and behavioral attributes predisposed the spray toads to chytridiomycosis, due to B. dendrobatidis infection, and how epidemic disease could have been exacerbated by altered environmental conditions in the spray wetlands. Our results show that chytridiomycosis was the proximate cause of extinction in the wild of N. asperginis. This represents the first known case of extinction by disease of an amphibian species in Africa. A captive breeding program in the US and Tanzania ensures the survival of the species and a reintroduction program is underway. However, we caution that chytridiomycosis remains an existing threat that requires a comprehensive mitigation strategy before the desired conservation outcome of an established population of repatriated toads can be achieved.

epidemiology↗

Temperature is a key driver of a wildlife epidemic and future warming will increase impacts

Increasing environmental temperatures are predicted to have increasingly severe and deleterious effects on biodiversity. For the most part, the impacts of a warming environment are presumed to be direct, however some predict increasingly severe disease epidemics, primarily from vector-borne pathogens, that will have the capacity to deplete host populations. Data to support this hypothesis are lacking. Here we describe increasing severity of ranavirosis driven by increasing temperature affecting a widely distributed amphibian host. Both in vitro and in vivo experiments showed that increasing environmental temperature leads to increased propagation of ranavirus and, in the latter, increased incidence of host infection and mortality. Also, temperature was shown to be a key determinant of disease dynamics in wild amphibians, raising the odds and severity of disease incidents. The direction of this effect was highly consistent in the context of other interacting variables such as shading around ponds. Projections based on future climate indicate that changes in seasonal weather in the UK will result in the increased incidence of severe cases of ranavirosis in amphibian populations that could affect recruitment. These complementary lines of evidence present a clear case of direct environmental modulation of a host-pathogen interaction and provide information for proposing mitigation actions.

epidemiology↗