Wolbachia Mosquitoes in Hawaii: Unsettled Science
On June 28, 2022, the Hawaii Board of Agriculture approved the addition of three mosquitoes to the List of Restricted Animals in anticipation of the planned biopesticide IIT experiment in Hawaii’s native bird habitats. The initial process for bringing these mosquitoes into the state has also begun, with the board approving the first species – the Southern House Mosquito (Culex quinquefasciatus), inoculated with strains of Wolbachia bacteria – for importation and immediate field release by permit.1
The project is called “Mosquito Control Research Using Wolbachia-based Incompatible Insect Technique” and is promoted as a population control effort to save Hawaii’s endangered native birds. The multi-agency partnership Birds, Not Mosquitoes, a steering committee formed in 2017 and comprised of state, federal, and non-governmental organizations, is coordinating the plan. Prior to the June 28th meeting, an exemption notice was signed by the Hawaii Board of Land and Natural Resources Chairperson Suzanne D. Case, stating that the Department of Land and Natural Resources (one of the lead agencies in the partnership) declares that this project will likely have minimum or no significant impact on the environment and is therefore exempt from the preparation of an environmental assessment.
With strong evidence of serious risks to public health and to the native birds targeted by this project, island residents are challenging the DLNR’s assertion and demanding a full scope Environmental Impact Study. Recent testimony shows that over 75% of the public is opposed to rushing forward with this experimental plan. Additional questions regarding invasive species control and conflicts of interest have been left unanswered by the state, and the task of researching and evaluating safety concerns now falls on the people. Our findings are alarming.
Of primary concern is the potential for increased pathogen infection due to non-sexual horizontal transmission of the introduced Wolbachia strains between the introduced biopesticide mosquitoes and the existing “wild” mosquitoes. Multiple factors are involved here, but first let’s look at the three mosquito species planned for import into Hawaii and just a few of the diseases they are known to transmit:
- The Southern House Mosquito (Culex quinquefasciatus) transmits avian malaria parasitic disease to birds and West Nile virus to both birds and humans.
- The Asian Tiger Mosquito (Aedes albopictus) transmits both dengue fever and Zika virus to humans.
- The Yellow Fever Mosquito (Aedes aegypti) transmits dengue fever and yellow fever to humans
Horizontal transmission is defined as the spread of an infectious agent from one group or individual to another, directly or indirectly. In the case of the host arthropods (insects) and the infectious agent of Wolbachia bacteria, the horizontal transmission referenced here would be non-sexual. Imported Wolbachia bacterium strains involved in this project include wAlbA, wAlbB, and wPip4. These newly introduced strains (referred to here as “X”) are not currently present within the corresponding Culex quinquefasciatus species of Hawaii’s established mosquito population.
Tropical disease expert Dr. Lorrin Pang agreed to speak with me (Tina Lia) as a private citizen to explain more about horizontal spread of disease and the risks involved with this project. Pang has authored over 75 publications in peer-reviewed medical journals covering a broad range of studies such as malaria, dengue, rabies, rat lungworm, and COVID. He’s been an advisor and voting member of the U.S. Congress Medical Research Program for the past several years, serving on committees for infectious diseases – many of which are mosquito-borne. From 1985-2005, he worked with the WHO and Walter Reed Institute’s Malaria Program, focusing on global malaria control efforts through interventions combining diagnostics, chemotherapeutics, vector control, and vaccine development. As a public health leader on the islands, he has mitigated mosquito-borne illnesses – including dengue and Zika – for over two decades. Pang was honored for his life-saving intervention in Hawaii’s dengue fever outbreak.
Dr. Pang has been compiling studies documenting horizontal Wolbachia bacterial spread, and he’s concerned about the potential for significant adverse outcomes of the state’s proposal:
“The intent to save rare birds is sound. If the project goes as planned, this would be a valuable tool for future interventions. However, with new life forms coming to the islands, there is too much potential for unexpected, dangerous, irreversible ‘evolutionary’ events. This is especially true when the new organisms cannot be contained to their target ecosystem. Already there are published papers pointing out the real threat of horizontal spread of the novel Wolbachia beyond the male Culex mosquito. The papers cover two general areas – the widespread detection of Wolbachia across so many diverse types of insects, and more recently, the growing number of reports of mechanisms of how this might occur. First, we all must agree that unintended horizontal spread of Wpip4 (imported strain) to, say, female Culex, Aedes mosquitoes (human disease vectors), or other insect vectors of diseases would be a catastrophe, and probably irreversible. Hawaii has a bad history of invasive species entering and spreading unabated, including their spread of infectious diseases.
Proponents may be right that this intervention will save the native birds in the short-term, but long-term consequences to other island ecologies and to these same native birds may ultimately be detrimental. When one realizes the latter, the damage may be impossible to recall or repair, like the effect we’ve seen with so many other invasive species in Hawaii.”
The safety assurances of the state’s biopesticide project are based heavily on the premise that only male mosquitoes will be released. Because the males are infected with an incompatible bacteria strain, when they mate with existing wild females, the offspring are not viable. However, Dr. Pang points to a more recent study out of Singapore2 describing Wolbachia bacteria strain “evolutionary associations” between mosquito hosts. The results of this mechanism widespread into diverse insect populations are not known. It may start with a few horizontal transfers to female mosquitoes. After that, the mating Wolbachia-X-compatible pair will quickly produce viable X offspring and spread the X bacteria strain (the term for this is “sweep”). If that were to happen here, the full capacity of those offspring to transmit disease would be unknown. This type of spread and sweep could also affect other insects, not just the targeted mosquito.
The combination of horizontal and vertical spread dramatically contradicts the state’s safety narrative. While the potential for accidental misidentification and release of lab-reared X-infected females (who bite and breed) has already been downplayed, the possibility of unintentionally producing these females in the wild has not been addressed at all. As Pang puts it,
“It is enough to say that the new Wolbachia strain can spread horizontally as a life form to other mosquitos (say Aedes, the vectors of human disease) and perhaps create that Wolbachia female Culex which everyone is bending over backwards to avoid via lab contamination.”
Dr. Pang further points out that there is a big difference between the standard Sterile Insect Technique (SIT) strategies used in the past that were based on radiation or chemicals, and the relatively new Incompatible Insect Technique (IIT). The mathematical models may be similar for estimating threshold criteria to affect mosquito population dynamics, but standard methods of sterility are not bacterial life forms that might escape horizontally and amplify in other ecological niches. According to Pang,
“While sterility models can predict the thresholds needed to exterminate a species (in this case insects), the radiation sterility factor (standard SIT) does not behave the same as a life form (i.e., Wpip4 Wolbachia bacteria). There may be different modeling between radiation and Wolbachia ‘sterility’ for the male mosquitoes, depending on male mosquito fitness – but more importantly, for the unintended female Culex to which the Wolbachia X spreads horizontally. How is this supposed to be self-contained? Horizontal spread has the potential to be a disaster that cannot be recalled. The bacterium is a life form, and you might not be able to turn back the clock by simply shutting off the male mosquito ‘fountains.’ ”
The evidence of horizontal spread of Wolbachia shows that the bacteria go not only to sexual cells, but also to somatic cells (non-sexual cells of the body). Wolbachia can also live outside of intra-cellular systems for several months.3 Dr. Pang emphasizes two additional studies documenting widespread horizontal transmission of Wolbachia. The first focuses on predatory wasps spreading the bacteria through contaminated mouth parts when feeding serially on target insects such as aphids4. Pang calls for more research into which predators, like the damselfly and dragonfly, sequentially feed on both male and female mosquitoes. This scenario might play out in either the predator of adults feeding on adult mosquitoes (X-infected and wild), or the X-infected predator of larva feeding on wild mosquito larva in common breeding sites. The second study looks at ant colonies spreading Wolbachia through the gastrointestinal (GI) tract when the ants feed on their fungus gardens.3 Pang asks an important question, “What about shared sugar feeding sites for X-infected male and wild adult male and female mosquitoes?” The sparser the sugar sites, the more communal interaction they will have. Dr. Pang finds these studies of horizontal transfer across species of insects worrisome, and says, “Even if this project achieved miraculous blocking of avian malaria to the native birds, what else would it do?”
To complicate matters more, the Wolbachia bacteria itself is parasitic, manipulating the reproductive biology of the host to increase its own transmission. Parasitic organisms can also alter the behavior of the hosts they live inside, and we just don’t know how this might play out in our native bird habitats. Will the X-infected mosquitoes or their offspring be capable of moving up to even higher elevations? Would they be more aggressive? How would increased pathogen infection and elevated capacity for disease transmission factor into these scenarios?
Consider the example posed by the article “Parasites brainwash grasshoppers into death dive,”5 where a parasitic worm brainwashes the grasshopper host it invades to jump into water and commit suicide. The parasite accomplishes this by chemically influencing the grasshopper’s brain, producing proteins which directly and indirectly affect the host’s central nervous system. This causes an altering of the grasshopper’s behavior so that it acts in a way it never usually would. Other parasites are noted as manipulators of their hosts’ behavior, including “enslaver” fungi that make their insect hosts die perched in a position that favors the dispersal of spores by the wind. It is widely believed that Wolbachia bacteria is such a parasite (intracellular) that modifies the mosquito host’s behaviors in ways we are only now beginning to understand.
There are far too many unknowns here, and this research project has the very real potential of further endangering Hawaii’s native bird populations – possibly even leading to their extinction and the extinction of native birds not currently threatened. Why the state would choose to proceed with an experimental population control technique with limited background information when there are alternatives available with decades of study behind them is unclear at this point. Supporters of this proposal seem to have good intentions with their focus on mosquito control to save the birds, but there appears to be a lack of awareness about the serious risks posed by horizontal transmission of the Wolbachia X-strain bacteria and the resulting consequences of that spread.
Hawaii is united in our support for conservation of the native birds that are vital to honoring and preserving the culture, history, and natural environment of the islands. This biopesticide IIT experiment is not the answer. With the understanding of the multiple dangers posed to our ecosystems, native birds, and public health, it is now time for all of the agencies involved in this plan to agree that it cannot be rushed forward. As one public testifier so clearly stated, “Hawaii is not a petri dish.” The public demands a full scope Environmental Impact Study. We will not allow the state to recklessly sidestep that crucial process.
End of Part 2
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- Board of Agriculture Meeting Agenda: Items IV.C.1 and IV.C.2 (06/28/2022) https://hdoa.hawaii.gov/wp-content/uploads/2022/06/06-28-22-AGENDA.pdf
- “Wolbachia infection in wild mosquitoes (Diptera: Culicidae): implications for transmission modes and host-endosymbiont associations in Singapore” – Huicong Ding, Huiqing Yeo, Nalini Puniamoorthy (BMC, 12/09/2020) https://parasitesandvectors.biomedcentral.com/articles/10.1186/s13071-020-04466-8
- “Wolbachia Horizontal Transmission Events in Ants: What Do We Know and What Can We Learn?” – Sarah J. A. Tolley, Peter Nonacs, Panagiotis Sapountzis (Frontiers in Microbiology, 03/06/2019) https://www.frontiersin.org/articles/10.3389/fmicb.2019.00296/full
- “The Intracellular Bacterium Wolbachia Uses Parasitoid Wasps as Phoretic Vectors for Efficient Horizontal Transmission” – Muhammad Z. Ahmed, Shao-Jian Li, Xia Xue, Xiang-Jie Yin, Shun-Xiang Ren, Francis M. Jiggins, Jaco M. Greeff, Bao-Li Qiu (National Center for Biotechnology Information, National Library of Medicine, 02/12/2015) https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4347858/
- “Parasites brainwash grasshoppers into death dive” – Shaoni Bhattacharya (New Scientist, 08/31/2005) https://www.newscientist.com/article/dn7927-parasites-brainwash-grasshoppers-into-death-dive/
“GENETIC DIVERSITY OF WOLBACHIA ENDOSYMBIONTS IN CULEX QUINQUEFASCIATUS FROM HAWAI’I, MIDWAY ATOLL AND AMERICAN SAMOA” – Carter T. Atkinson, William Watcher-Weatherwax, Dennis A. LaPointe (Hawaii Cooperative Studies Unit, UH at Hilo, 02/2016) https://dspace.lib.hawaii.edu/bitstream/10790/2671/TR074CarterWolbachia.pdf
“Infection of New- and Old-World Aedes albopictus (Diptera: Culicidae) by the Intracellular Parasite Wolbachia: Implications for Host Mitochondrial DNA Evolution” – Peter Armbruster, William E. Damsky, Jr., Rosanna Giordano, Josephine Birungi, Leonard E. Munstermann, Jan E. Conn (Journal of Medical Entomology, 05/01/2003) https://academic.oup.com/jme/article/40/3/356/877101
“Wolbachia” – Karine Prevot (The Embryo Project Encyclopedia, 01/29/2015) https://embryo.asu.edu/pages/wolbachia
“Sugar feeding patterns of New York Aedes albopictus mosquitoes are affected by saturation deficit, flowers, and host seeking” – Kara Fikrig, Sonile Peck, Peter Deckerman, Sharon Dang, Kimberly St Fleur, Henry Goldsmith, Sophia Qu, Hannah Rosenthal, Laura C. Harrington (PLOS Neglected Tropical Diseases, 10/26/2020) https://journals.plos.org/plosntds/article?id=10.1371/journal.pntd.0008244#:~:text=Sugar%20also%20may%20enhance%20male,%2Dseeking%20behavior%20%5B20%5D
“Plant-mediated interspecific horizontal transmission of an intracellular symbiont in insects” – Elena Gonella, Massimo Pajoro, Massimo Marzorati, Elena Crotti, Mauro Mandrioli, Marianna Pontini, Daniela Bulgari, Ilaria Negri, Luciano Sacchi, Bessem Chouaia, Daniele Daffonchio, Alberto Alma (Nature, Scientific Reports, 11/13/2015) https://www.nature.com/articles/srep15811
“Wolbachia Associations with Insects: Winning or Losing Against a Master Manipulator” – Claudia C. Correa, J. W. O. Ballard (Frontiers in Ecology and Evolution, 01/19/2016) https://www.frontiersin.org/articles/10.3389/fevo.2015.00153/full