Gut Bacteria Manipulation in Invasive Mosquitos
By T Schwab
Keywords: Biocontrol, Invasives, Extinction, Natives, Birds
Summary
In April 2023, the United States Environmental Protection Agency (EPA) approved an emergency exemption for the use of“DBQ Males”— male southern house mosquitoes (Culex quinquefasciatus) that have been infected with a novel Wolbachia pipientis bacteria strain labelled the DBQ strain. DBQ Males are to be released across Hawaii to mate with wild females who carry different or no Wolbachia strains resulting in infertile eggs (United States Environmental Protection Agency [EPA],2023). A potential site for the release of DBQ males includes the Alaka'i Wilderness Preserve (AWP) on the island of Kauaʻi. The AWP is home to the unique alpine bog and wet montane forest ecosystems which is the habit to multiple endangered bird species. Such bird species include the Akikiki (Oreomystis bairdi) and Akeke’e (Loxops caeruleirostris), both of which are down to under 1000 individuals and are under threat of avian malaria spread by mosquitoes. The use of the DBQ males to diminish invasive mosquito populations in the AWP gives hope to these native birds currently on the brink of extinction.
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Ecological genealogy
The Alaka'i Wilderness Preserve (AWP) is Hawaii’s first wilderness preserve consisting of 4,022 hectares of land set aside in 1964 from the Nā Pali-Kona Forest Reserve located on Kauaʻi island (Department of Land and Natural Resources, 2009). Found within this reserve is the Olokele Plateau found on the western side of Mount Waialeale—the island's highest point and remnants of the volcano that formed the island (Fricker et al., 2021). The eastern side of the original shield volcano slumped, causing a steep incline, so when northeast tradewinds that carry warm, moist air from the ocean meet this incline the air is brought up to high elevations of 1500 meters above sea level (Smok & Sedziak, n.d.; van’t Woudt & Nelson,1963). The sudden drop in temperature causes rain clouds to form, dumping an average of 11 meters of annual precipitation, making the Olokele Plateau one of the wettest places on Earth (Fricker et al., 2021. The resulting ecosystem is an alpine bog and wet montane forest, which comprise the Alakaiʻi swamp (van’t Woudt & Nelson,1963). This land has historically been used as a shortcut trail through the south shore of the Waimea region to the north (Hulme, 1965). And has been given the title of Alakaiʻi meaning “guide” “to lead” or “one-file track” in English according to different sources reflecting this historical use for travel (Hulme, 1965; Hawaii Aloha Travel Blog, n.d.; van’t Woudt & Nelson,1963). The Plateau and surrounding forests have long been home to rare and endemic species that thrive in this unique ecosystem. With 131 flowering plant species and 13 rare forest bird species historically found in the area (Boissoneault, 2021).
In 1826 invasive mosquito populations carrying avian malaria and avian pox spread across the Hawaiian islands. Species such as the southern house mosquito (Culex quinquefasciatus) carry both avian malaria and pox—pathogens that native birds have not built immunity to. Combined with other ecological threats such as predation from introduced rats, feral pigs and ungulates there was a dramatic decline in native Hawaiian bird populations up into the 1960s (Cannarella, 2010). 1969 marked the last observation of the Kaua‘i ‘akialoa (Hemignathus procerus)— a Hawaiian honeycreeper that was susceptible to Avian pox and last seen in the Alakaiʻi swamp before its extinction (Hawai‘i's State Wildlife Action Plan, 2015). An expedition in 1975 found a range contraction of all native Kauaʻi forest birds, who were now confined to the montane forests of the Plateau (Cannarella, 2010). The high elevation and cooler temperatures offered refuge from mosquito vectors — which require higher temperatures for their development (Atkinson & Lapointe, 2009). However, slowed rates of malaria and pox transmission were still seen, as all elevations of Kauaʻi are susceptible to transmission (Atkinson & Lapointe, 2009).
Hurricanes Iwa and Iniki in 1982 and 1992 respectively hit Kauaʻi, significantly impacting the forest structure (Behnke et al., 2014). The forest canopy was fragmented providing an opportunity for invasives such as Himalayan ginger (Hedychium gardnerianium) to encroach and out-compete native cover resulting in lower rates of native forest birds in invaded areas (Fricker et al., 2021). During this time the native Kauaʻi Oo (Moho braccatus), a Hawaiian honeyeater suited to the lower elevation of the Alakaiʻi forests sought refuge in upward elevations. In these higher elevations, the birds nested in the ʻŌhiʻa lehua (Metrosideros polymorpha) trees that were later damaged due to the hurricanes. Detrimental events such as these led to the extinction of the Kauaʻi Oo (Moho braccatus) (Division of Forestry and Wildlife [DFW], 2024). In the following decades, 3 other native species of birds also became extinct in the AWP (Boissoneault, 2021).
In 1826 invasive mosquito populations carrying avian malaria and avian pox spread across the Hawaiian islands. Species such as the southern house mosquito (Culex quinquefasciatus) carry both avian malaria and pox—pathogens that native birds have not built immunity to. Combined with other ecological threats such as predation from introduced rats, feral pigs and ungulates there was a dramatic decline in native Hawaiian bird populations up into the 1960s (Cannarella, 2010). 1969 marked the last observation of the Kaua‘i ‘akialoa (Hemignathus procerus)— a Hawaiian honeycreeper that was susceptible to Avian pox and last seen in the Alakaiʻi swamp before its extinction (Hawai‘i's State Wildlife Action Plan, 2015). An expedition in 1975 found a range contraction of all native Kauaʻi forest birds, who were now confined to the montane forests of the Plateau (Cannarella, 2010). The high elevation and cooler temperatures offered refuge from mosquito vectors — which require higher temperatures for their development (Atkinson & Lapointe, 2009). However, slowed rates of malaria and pox transmission were still seen, as all elevations of Kauaʻi are susceptible to transmission (Atkinson & Lapointe, 2009).
Hurricanes Iwa and Iniki in 1982 and 1992 respectively hit Kauaʻi, significantly impacting the forest structure (Behnke et al., 2014). The forest canopy was fragmented providing an opportunity for invasives such as Himalayan ginger (Hedychium gardnerianium) to encroach and out-compete native cover resulting in lower rates of native forest birds in invaded areas (Fricker et al., 2021). During this time the native Kauaʻi Oo (Moho braccatus), a Hawaiian honeyeater suited to the lower elevation of the Alakaiʻi forests sought refuge in upward elevations. In these higher elevations, the birds nested in the ʻŌhiʻa lehua (Metrosideros polymorpha) trees that were later damaged due to the hurricanes. Detrimental events such as these led to the extinction of the Kauaʻi Oo (Moho braccatus) (Division of Forestry and Wildlife [DFW], 2024). In the following decades, 3 other native species of birds also became extinct in the AWP (Boissoneault, 2021).
Present Tense
The State of Hawaii’s Department of Land and Natural Resources continues to manage the AWP. The land's main use is preservation with access to the site limited to on foot through different hiking trails. In the 1990’s a boardwalk was installed across the preserve and in 2016 trail improvements were made (Hawaii Aloha Travel Blog, n.d). The AWP is now home to 8 of the 13 species of native birds historically seen in the area (Boissoneault, 2021). Such native forest birds include the endemic Hawaiian honeycreeper Akeke’e (Loxops caeruleirostris)—with a population of less than 1,000 individuals (Boissoneault, 2021). As well as, the Akikiki (Oreomystis bairdi) another Hawaiian honeycreeper endemic to Kauaʻi with an estimated population of under 500 individuals (Boissoneault, 2021). Akikiki (Oreomystis bairdi) was once found in lower elevations relying on the materials of dead trees such as koa (Acacia koa), however, has moved to upward elevations away from koa forests and into large ʻŌhiʻa lehua (Metrosideros polymorpha) forests for nesting (Fricker et al., 2021), much like the extinct Kauaʻi Oo (Moho braccatus). Unprecedented rates of warming are causing native bird species to seek higher elevations for refuge from mosquito vectors. (Atkinson & Lapointe, 2009). However, like the extinct Kauaʻi Oo (Moho braccatus) these species are often less fit for these higher elevations, making them more prone to population decline in the face of varying risks/stressors. Both Akeke’e (Loxops caeruleirostris) and Akikiki (Oreomystis bairdi) are susceptible to avian malaria (Fricker et al., 2021). While, the endangered Puaiohi (Myadestes palmeri) endemic to Kauaʻi is relatively tolerant of avian malaria and is instead most affected by the degradation of their native ecosystem by the invasive strawberry guava (Psidium cattleianum) and fire tree (Myrica faya) (DFW, 2024). The AWP has many efforts in effect to ensure the survival of these rare endemic birds. The implementation of pig fencing and the setting of rat traps attempt to address predatory invasive species (Behnke et al., 2014). Other projects have included the introduction of BTI (Bacillus thuringiensis israelensis) bacteria into streams to kill mosquito larvae with the ecological impact of killing a few midge species (Boissoneault, 2021).
In April of 2023, the United States Environmental Protection Agency (EPA) approved an emergency exemption for the use of “DBQ Males” across conservation sites on the Hawaiian Islands (United States Environmental Protection Agency [EPA],2023). These DBQ males are male southern house mosquitoes (Culex quinquefasciatus) that have been infected with a novel Wolbachia pipientis bacteria strain labelled the DBQ strain. Wolbachia is a naturally forming endosymbiotic bacteria that lives in the cells of its hosts. The introduction of the novel strain causes cytoplasmic incompatibility between infected males and uninfected females with differing or no Wolbachia strains (EPA,2023). DBQ male sperm is no longer compatible with the female egg cytoplasm resulting in eggs that never hatch.
In April of 2023, the United States Environmental Protection Agency (EPA) approved an emergency exemption for the use of “DBQ Males” across conservation sites on the Hawaiian Islands (United States Environmental Protection Agency [EPA],2023). These DBQ males are male southern house mosquitoes (Culex quinquefasciatus) that have been infected with a novel Wolbachia pipientis bacteria strain labelled the DBQ strain. Wolbachia is a naturally forming endosymbiotic bacteria that lives in the cells of its hosts. The introduction of the novel strain causes cytoplasmic incompatibility between infected males and uninfected females with differing or no Wolbachia strains (EPA,2023). DBQ male sperm is no longer compatible with the female egg cytoplasm resulting in eggs that never hatch.
Future Trajectory
Preliminary studies have supported the emergency use of DBQ Males at the AWP for the restoration of native bird populations endangered by avian pathogens. Such studies have found there are little to no detrimental effects associated with their introduction and have begun education public hearings on their use (Crampton et al., 2021). The emergency use of these DBQ males has been credited to climate-change-induced temperatures in Hawaii (EPA,2023). Rising temperatures and lower precipitation facilitate favorable larval mosquito habitats resulting in the contracting of native bird ranges to higher elevations with cooler temperatures (Berio Fortini et al., 2020). As the climate continues to warm these areas will no longer exist creating the need to address Culex quinquefasciatus populations now before they drive these native birds to extinction. The EPA has approved the deployment of up to 156,000,000 DBQ males per year across conservation sites (EPA, 2023). Estimated data suggests that the AWP requires 1.5 million DBQ Males to be released each week (Vorsino & Xi, 2022). The release of these DBQ males across the AWP will cost an estimated $1.16 million in its first year for startup lab and equipment costs with a projected $376,000 yearly budget to follow (Vorsino & Xi, 2022). As of December 2023, this project is currently underway and is seeking renewal for another year (Department of Agriculture).
This marks the first project that has made use of DBQ males for bird restoration, as they have been used previously to address pathogens affecting humans (Boissoneault, 2021). While the introduction of novel Wolbachia bacteria into ecosystems is labelled as low-risk, this is still largely experimental meaning the long-term effects of these mosquitos are largely unknown. Wolbachia has been found to enhance rates of infection such as the West Nile Virus in other species of mosquitoes, making it a possibility in Culex quinquefasciatus. To address these concerns the DBQ males must undergo an extensive manufacturing process that tests for any pathogens before release (EPA,2023). This extensive manufacturing process also regulates the number of accidental females released, as male Culex quinquefasciatus primarily feeds on nectar while females feed on blood (EPA,2023). It is these accidentally released females that have brought up concern for human health, and while this species of mosquito shows to have no detrimental effects on human populations it’s an important ethical consideration to inform local communities about this project. Being the first of its kind, this project will likely inspire more like it and as such its manufacturing process will likely set a framework for the use of DBQ males in other natures.
This marks the first project that has made use of DBQ males for bird restoration, as they have been used previously to address pathogens affecting humans (Boissoneault, 2021). While the introduction of novel Wolbachia bacteria into ecosystems is labelled as low-risk, this is still largely experimental meaning the long-term effects of these mosquitos are largely unknown. Wolbachia has been found to enhance rates of infection such as the West Nile Virus in other species of mosquitoes, making it a possibility in Culex quinquefasciatus. To address these concerns the DBQ males must undergo an extensive manufacturing process that tests for any pathogens before release (EPA,2023). This extensive manufacturing process also regulates the number of accidental females released, as male Culex quinquefasciatus primarily feeds on nectar while females feed on blood (EPA,2023). It is these accidentally released females that have brought up concern for human health, and while this species of mosquito shows to have no detrimental effects on human populations it’s an important ethical consideration to inform local communities about this project. Being the first of its kind, this project will likely inspire more like it and as such its manufacturing process will likely set a framework for the use of DBQ males in other natures.
References
Atkinson, C. T., & Lapointe, D. A.. (2009). Introduced Avian Diseases, Climate Change, and the Future of Hawaiian Honeycreepers. Journal of Avian Medicine and Surgery, 23(1), 53–63. https://doi.org/10.1647/2008-059.1
Behnke, L.A.H. Goldstein, L., Crampton, L., Angeloni, L., & Theobald, D.(2014). Habitat use and Conservation Implications for Akikiki (Oreomytis bairdi) and Akekee (Loxops caeruleirostris), Two Endagnered Hawaiian Honeycreepers. [Masters Thesis, Colorado State University]. Mountainscholar.org. https://api.mountainscholar.org/server/api/core/bitstreams/2cb6850c-a03a-4a34-b705-d5961cdbc7d6/content
Berio Fortini, L., Kaiser, L. R., & LaPointe, D. A. (2020). Fostering real-time climate adaptation: Analyzing past, current, and forecast temperature to understand the dynamic risk to Hawaiian honeycreepers from avian malaria. Global Ecology and Conservation, 23, e01069. https://doi.org/10.1016/j.gecco.2020.e01069
Boissoneault, L. (2021, November 4). Mosquitoes to the Rescue! The Last-Ditch Effort to Save Kaua‘i’s Endangered Birds. Audubon. https://www.audubon.org/news/mosquitoes-rescue-last-ditch-effort-save-kauais-endangered-birds
Cannarella, R. (2010). Appendix F: Timeline of Forest history in Hawaii.Hawaii Division
of Forestry and Wildlife. https://dlnr.hawaii.gov/forestry/files/2013/09/Appendix-F-Forest-History.pdf
Crampton, L., Cabera, A., Gilb, R.,Vorsino, A., Berry, L. (2021, March 29). Laying the Groundwork for Landscape-level Mosquito Suppression to Protect Endangered Forest Birds and Human Health from Mosquito Borne Disease in Hawaii. University of Hawaii Pacific Cooperative Studies Unit Kauaʻi Forest Bird Recovery Project. https://kauaiforestbirds.org/wp-content/uploads/2021/04/HISC-FY20-Final-Report_Laying-the-groundwork-for-mosquito-control.pdf
Department of Agriculture. (2023). Request for Renewal of Exemption of Federal and State Agencies for Use of a Pesticide Under Emergency Conditions (23HI01). State of Hawaii.file:///C:/Users/there/Downloads/EPA-HQ-OPP-2024-0035-0003_contentpdf
Department of Land and Natural Resources (2009, November). Nā Pali-Kona Forest Reserve. https://dlnr.hawaii.gov/forestry/frs/reserves/kauai/na-pali-kona/
Division of Forestry and Wildlife. (2024). Kaua‘i ‘ō ‘ō. https://dlnr.hawaii.gov/wildlife/birds/kauai-oo/
Division of Forestry and Wildlife. (2024). Puaiohi. https://dlnr.hawaii.gov/wildlife/birds/puaiohi/
Fricker, G. A., Crampton, L. H., Gallerani, E. M., Hite, J. M., Inman, R., & Gillespie, T. W. (2021). Application of lidar for critical endangered bird species conservation on the island of Kauai, Hawaii. Ecosphere, 12(6), e03554. https://doi.org/10.1002/ecs2.3554
Hawaii Aloha Travel Blog.(n.d.). Hiking Through Kauai’s Alakaʻi Wilderness Preserve. Hawaii Aloha Travel Blog. https://www.hawaii-aloha.com/blog/kauais-alakai-swamp-trail-raw-native-nature/
Hawaiian Islands.com (n.d.). The Alakai Wilderness Preserve: The Remote Heart of Kauai's Alakai Swamp. Hawaiian Islands.com. https://hawaiianislands.com/kauai/things-to-do/alakai-wilderness-preserve
Hawai‘i's State Wildlife Action Plan. (2015, October 1). Forest Birds: Kaua‘i ‘akialoa. Hawaii Government. https://dlnr.hawaii.gov/wildlife/files/2019/03/SWAP-2015-Kauai-akialoa-Final.pdf
Hulme, K.C. (1965, January). The Timeless Kauaʻi Swamp.The Atlantic.https://www.theatlantic.com/magazine/archive/1965/01/the-timeless-kauai-swamp/660086/
Memorandium, Section 18 – Specific Exemption for use of DQB Males on Conservation Areas to Control Culex quinquefasciatus mosquitoes in Hawaii (EE# 23HI01) (2023). file:///C:/Users/there/Downloads/EPA-HQ-OPP-2022-0896-0265_content.pdf
Smok, M. & Sedziak (n.d.) Alaka'i Swamp Hike: Pihea Trail &Alaka'i Swamp Trail to
Kilohana Lookout. Travellibn.com. https://www.travelibn.com/alakai-swamp-hike
United States Environmental Protection Agency (2023,April 27). EPA Approves Emergency Exemption for Wolbachia Mosquitoes to Protect Endangered Birds in Hawaii. https://www.epa.gov/pesticides/epa-approves-emergency-exemption-wolbachia-mosquitoes-protect-endangered-bird-hawaii#:~:text=This%20week%2C%20the%20U.S.%20Environmental,contributing%20to%20endangered%20bird%20species
van't Woudt, Bessel D .& Nelson, Robert E. (1963). Hydrology of the Alakai Swamp, Kauai, Hawaii. Hawaii Agricultural Experimental Station Bulletin, 132, 7-30. http://hdl.handle.net/10125/15285
Vorsino, A. E., & Xi, Z.. (2022). A mass rearing cost calculator for the control of Culex quinquefasciatus in Hawaiʻi using the incompatible insect technique. Parasites & Vectors, 15(1). https://doi.org/10.1186/s13071-022-05522-1
Behnke, L.A.H. Goldstein, L., Crampton, L., Angeloni, L., & Theobald, D.(2014). Habitat use and Conservation Implications for Akikiki (Oreomytis bairdi) and Akekee (Loxops caeruleirostris), Two Endagnered Hawaiian Honeycreepers. [Masters Thesis, Colorado State University]. Mountainscholar.org. https://api.mountainscholar.org/server/api/core/bitstreams/2cb6850c-a03a-4a34-b705-d5961cdbc7d6/content
Berio Fortini, L., Kaiser, L. R., & LaPointe, D. A. (2020). Fostering real-time climate adaptation: Analyzing past, current, and forecast temperature to understand the dynamic risk to Hawaiian honeycreepers from avian malaria. Global Ecology and Conservation, 23, e01069. https://doi.org/10.1016/j.gecco.2020.e01069
Boissoneault, L. (2021, November 4). Mosquitoes to the Rescue! The Last-Ditch Effort to Save Kaua‘i’s Endangered Birds. Audubon. https://www.audubon.org/news/mosquitoes-rescue-last-ditch-effort-save-kauais-endangered-birds
Cannarella, R. (2010). Appendix F: Timeline of Forest history in Hawaii.Hawaii Division
of Forestry and Wildlife. https://dlnr.hawaii.gov/forestry/files/2013/09/Appendix-F-Forest-History.pdf
Crampton, L., Cabera, A., Gilb, R.,Vorsino, A., Berry, L. (2021, March 29). Laying the Groundwork for Landscape-level Mosquito Suppression to Protect Endangered Forest Birds and Human Health from Mosquito Borne Disease in Hawaii. University of Hawaii Pacific Cooperative Studies Unit Kauaʻi Forest Bird Recovery Project. https://kauaiforestbirds.org/wp-content/uploads/2021/04/HISC-FY20-Final-Report_Laying-the-groundwork-for-mosquito-control.pdf
Department of Agriculture. (2023). Request for Renewal of Exemption of Federal and State Agencies for Use of a Pesticide Under Emergency Conditions (23HI01). State of Hawaii.file:///C:/Users/there/Downloads/EPA-HQ-OPP-2024-0035-0003_contentpdf
Department of Land and Natural Resources (2009, November). Nā Pali-Kona Forest Reserve. https://dlnr.hawaii.gov/forestry/frs/reserves/kauai/na-pali-kona/
Division of Forestry and Wildlife. (2024). Kaua‘i ‘ō ‘ō. https://dlnr.hawaii.gov/wildlife/birds/kauai-oo/
Division of Forestry and Wildlife. (2024). Puaiohi. https://dlnr.hawaii.gov/wildlife/birds/puaiohi/
Fricker, G. A., Crampton, L. H., Gallerani, E. M., Hite, J. M., Inman, R., & Gillespie, T. W. (2021). Application of lidar for critical endangered bird species conservation on the island of Kauai, Hawaii. Ecosphere, 12(6), e03554. https://doi.org/10.1002/ecs2.3554
Hawaii Aloha Travel Blog.(n.d.). Hiking Through Kauai’s Alakaʻi Wilderness Preserve. Hawaii Aloha Travel Blog. https://www.hawaii-aloha.com/blog/kauais-alakai-swamp-trail-raw-native-nature/
Hawaiian Islands.com (n.d.). The Alakai Wilderness Preserve: The Remote Heart of Kauai's Alakai Swamp. Hawaiian Islands.com. https://hawaiianislands.com/kauai/things-to-do/alakai-wilderness-preserve
Hawai‘i's State Wildlife Action Plan. (2015, October 1). Forest Birds: Kaua‘i ‘akialoa. Hawaii Government. https://dlnr.hawaii.gov/wildlife/files/2019/03/SWAP-2015-Kauai-akialoa-Final.pdf
Hulme, K.C. (1965, January). The Timeless Kauaʻi Swamp.The Atlantic.https://www.theatlantic.com/magazine/archive/1965/01/the-timeless-kauai-swamp/660086/
Memorandium, Section 18 – Specific Exemption for use of DQB Males on Conservation Areas to Control Culex quinquefasciatus mosquitoes in Hawaii (EE# 23HI01) (2023). file:///C:/Users/there/Downloads/EPA-HQ-OPP-2022-0896-0265_content.pdf
Smok, M. & Sedziak (n.d.) Alaka'i Swamp Hike: Pihea Trail &Alaka'i Swamp Trail to
Kilohana Lookout. Travellibn.com. https://www.travelibn.com/alakai-swamp-hike
United States Environmental Protection Agency (2023,April 27). EPA Approves Emergency Exemption for Wolbachia Mosquitoes to Protect Endangered Birds in Hawaii. https://www.epa.gov/pesticides/epa-approves-emergency-exemption-wolbachia-mosquitoes-protect-endangered-bird-hawaii#:~:text=This%20week%2C%20the%20U.S.%20Environmental,contributing%20to%20endangered%20bird%20species
van't Woudt, Bessel D .& Nelson, Robert E. (1963). Hydrology of the Alakai Swamp, Kauai, Hawaii. Hawaii Agricultural Experimental Station Bulletin, 132, 7-30. http://hdl.handle.net/10125/15285
Vorsino, A. E., & Xi, Z.. (2022). A mass rearing cost calculator for the control of Culex quinquefasciatus in Hawaiʻi using the incompatible insect technique. Parasites & Vectors, 15(1). https://doi.org/10.1186/s13071-022-05522-1