The direct and indirect effects of copper on vector-borne disease dynamics

Neff, Erik; Dharmarajan, Guha

doi:10.1016/j.envpol.2020.116213

The direct and indirect effects of copper on vector-borne disease dynamics

Journal Article · Wed Dec 02 00:00:00 EST 2020 · Environmental Pollution

DOI:https://doi.org/10.1016/j.envpol.2020.116213· OSTI ID:1848959

Neff, Erik ^[1]; Dharmarajan, Guha ^[2]

Savannah River Site (SRS), Aiken, SC (United States). Savannah River Ecology Lab. (SREL); Univ. of Georgia, Athens, GA (United States). Warnell School of Forestry and Natural Resources; Savannah River Site (SRS), Aiken, SC (United States)
Savannah River Site (SRS), Aiken, SC (United States). Savannah River Ecology Lab. (SREL)

Metal pollution is a growing concern that affects the health of humans and animals globally. Copper is an essential insect micronutrient required for respiration, pigmentation and oxidative stress protection but can also act as a potentially toxic trace element. While several studies have focused on the negative fitness effects of copper on the aquatic larvae of mosquitoes, the effects of larval copper exposure on adult mosquito fitness (i.e., survival and fecundity) and their ability to transmit parasites (i.e., vector competence) remains unclear. Here, using a well-studied model vector-parasite system, the mosquito Aedes aegypti and parasite Dirofilaria immitis, we show that sublethal copper exposure in larval mosquitoes alters adult female fecundity and vector competence. Specifically, mosquitoes exposed to copper had a hormetic fecundity response and mosquitoes exposed to 600 μg/L of copper had significantly fewer infective parasite larvae than control mosquitoes not exposed to copper. Therefore, exposure of mosquito larvae to copper levels far below EPA-mandated safe drinking water limits (1300 μg/L) can impact vector-borne disease dynamics not only by reducing mosquito abundance (through increased larval mortality), but also by reducing parasite transmission risk. Our results also demonstrated that larval copper is retained through metamorphosis to adulthood in mosquitoes, indicating that these insects could transfer copper from aquatic to terrestrial foodwebs, especially in urban areas where they are abundant. To our knowledge this is the first study to directly link metal exposure with vector competence (i.e., ability to transmit parasites) in any vector-parasite system. Additionally, it also demonstrates unequivocally that mosquitoes can transfer contaminants from aquatic to terrestrial ecosystems. These results have broad implications for public health because they directly linking contaminants and vector-borne disease dynamics, as well as linking mosquitoes and contaminant dynamics.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of Georgia, Athens, GA (United States)

Sponsoring Organization:: USDOE; USDOE Office of Environmental Management (EM)

Grant/Contract Number:: EM0004391

OSTI ID:: 1848959

Alternate ID(s):: OSTI ID: 1777583

Journal Information:: Environmental Pollution, Journal Name: Environmental Pollution Journal Issue: C Vol. 269; ISSN 0269-7491

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

References (82)

In a state of flux: The energetic pathways that move contaminants from aquatic to terrestrial environments Sullivan, S. Mažeika P.; Rodewald, Amanda D. Environmental Toxicology and Chemistry, Vol. 31, Issue 6 https://doi.org/10.1002/etc.1842	journal	May 2012
Delayed effects and complex life cycles: How the larval aquatic environment influences terrestrial performance and survival: Delayed effects and complex life cycles Rumrill, Caitlin T.; Scott, David E.; Lance, Stacey L. Environmental Toxicology and Chemistry, Vol. 37, Issue 10 https://doi.org/10.1002/etc.4228	journal	August 2018
Effect of Heavy Metals onAedes aegypti(Diptera:Culicidae) Larvae Rayms-Keller, A.; Olson, K. E.; McGaw, M. Ecotoxicology and Environmental Safety, Vol. 39, Issue 1 https://doi.org/10.1006/eesa.1997.1605	journal	January 1998
Bioaccumulation of cadmium, lead, copper, and zinc in successive developmental stages of Lymantria dispar L. (Lymantriidae, Lepid)?a life cycle study Gintenreiter, S.; Ortel, J.; Nopp, H. J. Archives of Environmental Contamination and Toxicology, Vol. 25, Issue 1 https://doi.org/10.1007/BF00230711	journal	July 1993
Potential significance of insects in the removal of contaminants from aquatic systems Menzie, Charles A. Water, Air, and Soil Pollution, Vol. 13, Issue 4 https://doi.org/10.1007/BF02191848	journal	December 1980
Differential Toxicity to Cd, Pb, and Cu in Dragonfly Larvae (Insecta: Odonata) Tollett, V. D.; Benvenutti, E. L.; Deer, L. A. Archives of Environmental Contamination and Toxicology, Vol. 56, Issue 1 https://doi.org/10.1007/s00244-008-9170-1	journal	April 2008
Nematode and mercury content in freshwater fish belonging to different trophic levels Olivero-Verbel, Jesus; Caballero-Gallardo, Karina Parasitology Research, Vol. 112, Issue 6 https://doi.org/10.1007/s00436-013-3378-3	journal	March 2013
Disease-Driven Amphibian Declines Alter Ecosystem Processes in a Tropical Stream Whiles, M. R.; Hall, R. O.; Dodds, W. K. Ecosystems, Vol. 16, Issue 1 https://doi.org/10.1007/s10021-012-9602-7	journal	November 2012
Disease Ecology Meets Ecosystem Science Preston, Daniel L.; Mischler, John A.; Townsend, Alan R. Ecosystems, Vol. 19, Issue 4 https://doi.org/10.1007/s10021-016-9965-2	journal	February 2016
Methylmercury levels in a parasite (Apophallus brevis metacercariae) and its host, yellow perch (Perca flavescens) Ryman, Jennie E.; Van Walleghem, Jillian L. A.; Blanchfield, Paul J. Aquatic Ecology, Vol. 42, Issue 3 https://doi.org/10.1007/s10452-007-9104-4	journal	June 2007
Dietary (periphyton) and aqueous Zn bioaccumulation dynamics in the mayfly Centroptilum triangulifer Kim, K. S.; Funk, D. H.; Buchwalter, D. B. Ecotoxicology, Vol. 21, Issue 8 https://doi.org/10.1007/s10646-012-0985-1	journal	July 2012
The biogeochemical cycling of elemental mercury: Anthropogenic influences Mason, R. P.; Fitzgerald, W. F.; Morel, F. M. M. Geochimica et Cosmochimica Acta, Vol. 58, Issue 15 https://doi.org/10.1016/0016-7037(94)90046-9	journal	August 1994
Ultrastructure of Malpighian tubules of Aedes aegypti infected with Dirofilaria immitis Palmer, Catherine A.; Wittrock, Darwin D.; Christensen, Bruce M. Journal of Invertebrate Pathology, Vol. 48, Issue 3 https://doi.org/10.1016/0022-2011(86)90059-5	journal	November 1986
Hormesis — The stimulation of growth by low levels of inhibitors Stebbing, A. R. D. Science of The Total Environment, Vol. 22, Issue 3 https://doi.org/10.1016/0048-9697(82)90066-3	journal	February 1982
The fate of trace metals during the metamorphosis of chironomids (diptera, chironomidae) Timmermans, Klaas R.; Walker, Paddy A. Environmental Pollution, Vol. 62, Issue 1 https://doi.org/10.1016/0269-7491(89)90097-3	journal	January 1989
Oxidative mechanisms in the toxicity of metal ions Stohs, S. Free Radical Biology and Medicine, Vol. 18, Issue 2 https://doi.org/10.1016/0891-5849(94)00159-H	journal	February 1995
Competence of Aedes albopictus and Culex quinquefasciatus as vector of Dirofilaria immitis after blood meal with different microfilarial density Lai, Cheng-Hung; Tung, Kwong-Chung; Ooi, Hong-Kean Veterinary Parasitology, Vol. 90, Issue 3 https://doi.org/10.1016/S0304-4017(00)00242-9	journal	June 2000
Atmospheric mercury—An overview Schroeder, William H.; Munthe, John Atmospheric Environment, Vol. 32, Issue 5 https://doi.org/10.1016/S1352-2310(97)00293-8	journal	March 1998
Metallothioneins in aquatic invertebrates: Their role in metal detoxification and their use as biomarkers Amiard, J.; Amiardtriquet, C.; Barka, S. Aquatic Toxicology, Vol. 76, Issue 2 https://doi.org/10.1016/j.aquatox.2005.08.015	journal	February 2006
Pollution and parasitism in aquatic animals: A meta-analysis of effect size Blanar, Christopher A.; Munkittrick, Kelly R.; Houlahan, Jeff Aquatic Toxicology, Vol. 93, Issue 1 https://doi.org/10.1016/j.aquatox.2009.03.002	journal	June 2009
How micronutrients influence the physiology of mosquitoes Rivera-Pérez, Crisalejandra; Clifton, Mark E.; Noriega, Fernando G. Current Opinion in Insect Science, Vol. 23 https://doi.org/10.1016/j.cois.2017.07.002	journal	October 2017
Variation in Tolerance to Parasites Affects Vectorial Capacity of Natural Asian Tiger Mosquito Populations Dharmarajan, Guha; Walker, Kathryne D.; Lehmann, Tovi Current Biology, Vol. 29, Issue 22 https://doi.org/10.1016/j.cub.2019.09.047	journal	November 2019
Heartworm Biology, Treatment, and Control Bowman, Dwight D.; Atkins, Clarke E. Veterinary Clinics of North America: Small Animal Practice, Vol. 39, Issue 6 https://doi.org/10.1016/j.cvsm.2009.06.003	journal	November 2009
Heavy metals in mosquito larval habitats in urban Kisumu and Malindi, Kenya, and their impact Mireji, Paul O.; Keating, Joseph; Hassanali, Ahmed Ecotoxicology and Environmental Safety, Vol. 70, Issue 1 https://doi.org/10.1016/j.ecoenv.2007.03.012	journal	May 2008
Heavy metal pollution in surface water and sediment: A preliminary assessment of an urban river in a developing country Islam, Md Saiful; Ahmed, Md Kawser; Raknuzzaman, Mohammad Ecological Indicators, Vol. 48 https://doi.org/10.1016/j.ecolind.2014.08.016	journal	January 2015
Effects of heavy metals on population growth and metallothionein gene expression in the mosquito Culex quinquefasciatus, from Calcutta, India Sarkar, Sagartirtha; Duttagupta, Asish K.; Mal, Tarun K. Environmental Pollution, Vol. 127, Issue 2 https://doi.org/10.1016/j.envpol.2003.08.005	journal	January 2004
Trophic transfer and biotransformation of selenium in the mosquito (Aedes albopictus) and interactive effects with hexavalent chromium Zhou, Chuanqi; Huang, Jung-Chen; Zheng, Lixin Environmental Pollution, Vol. 262 https://doi.org/10.1016/j.envpol.2020.114288	journal	July 2020
Vector competence of Aedes aegypti mosquitoes for filarial nematodes is affected by age and nutrient limitation Ariani, Cristina V.; Juneja, Punita; Smith, Sophia Experimental Gerontology, Vol. 61 https://doi.org/10.1016/j.exger.2014.11.001	journal	January 2015
Parasites as drivers of key processes in aquatic ecosystems: Facts and future directions Sures, B.; Nachev, M.; Pahl, M. Experimental Parasitology, Vol. 180 https://doi.org/10.1016/j.exppara.2017.03.011	journal	September 2017
Characterization of cDNAs encoding putative laccase-like multicopper oxidases and developmental expression in the tobacco hornworm, Manduca sexta, and the malaria mosquito, Anopheles gambiae Dittmer, Neal T.; Suderman, Richard J.; Jiang, Haobo Insect Biochemistry and Molecular Biology, Vol. 34, Issue 1 https://doi.org/10.1016/j.ibmb.2003.08.003	journal	January 2004
Insect multicopper oxidases: Diversity, properties, and physiological roles Dittmer, Neal T.; Kanost, Michael R. Insect Biochemistry and Molecular Biology, Vol. 40, Issue 3 https://doi.org/10.1016/j.ibmb.2010.02.006	journal	March 2010
Global risk mapping for major diseases transmitted by Aedes aegypti and Aedes albopictus Leta, Samson; Beyene, Tariku Jibat; De Clercq, Eva M. International Journal of Infectious Diseases, Vol. 67 https://doi.org/10.1016/j.ijid.2017.11.026	journal	February 2018
Fate of blood meal iron in mosquitoes Zhou, Guoli; Kohlhepp, Pete; Geiser, Dawn Journal of Insect Physiology, Vol. 53, Issue 11 https://doi.org/10.1016/j.jinsphys.2007.06.009	journal	November 2007
Aedes aegypti pharate 1st instar quiescence affects larval fitness and metal tolerance Perez, Mario H.; Noriega, Fernando G. Journal of Insect Physiology, Vol. 58, Issue 6 https://doi.org/10.1016/j.jinsphys.2012.03.005	journal	June 2012
Toward a unified theory of caloric restriction and longevity regulation Sinclair, David A. Mechanisms of Ageing and Development, Vol. 126, Issue 9 https://doi.org/10.1016/j.mad.2005.03.019	journal	September 2005
Melanization immune responses in mosquito vectors Christensen, Bruce M.; Li, Jianyong; Chen, Cheng-Chen Trends in Parasitology, Vol. 21, Issue 4 https://doi.org/10.1016/j.pt.2005.02.007	journal	April 2005
Parasites and Their Impact on Ecosystem Nutrient Cycling Vannatta, J. Trevor; Minchella, Dennis J. Trends in Parasitology, Vol. 34, Issue 6 https://doi.org/10.1016/j.pt.2018.02.007	journal	June 2018
Metal accumulation in sediments and amphipods downstream of combined sewer overflows Schertzinger, Gerhard; Ruchter, Nadine; Sures, Bernd Science of The Total Environment, Vol. 616-617 https://doi.org/10.1016/j.scitotenv.2017.10.199	journal	March 2018
Effects of methylmercury on mosquito oviposition behavior: Maladaptive response to non-toxic exposure Neff, Erik; Coleman, Austin L.; Maness, Ryne W. Science of The Total Environment, Vol. 667 https://doi.org/10.1016/j.scitotenv.2019.02.314	journal	June 2019
Metal accumulation in riverine macroinvertebrates from a platinum mining region Erasmus, J. H.; Malherbe, W.; Zimmermann, S. Science of The Total Environment, Vol. 703 https://doi.org/10.1016/j.scitotenv.2019.134738	journal	February 2020
Hormesis: Highly Generalizable and Beyond Laboratory Agathokleous, Evgenios; Kitao, Mitsutoshi; Calabrese, Edward J. Trends in Plant Science, Vol. 25, Issue 11 https://doi.org/10.1016/j.tplants.2020.05.006	journal	November 2020
Is a healthy ecosystem one that is rich in parasites? Hudson, Peter J.; Dobson, Andrew P.; Lafferty, Kevin D. Trends in Ecology & Evolution, Vol. 21, Issue 7 https://doi.org/10.1016/j.tree.2006.04.007	journal	July 2006
Fine-scale temperature fluctuation and modulation of Dirofilaria immitis larval development in Aedes aegypti Ledesma, Nicholas; Harrington, Laura Veterinary Parasitology, Vol. 209, Issue 1-2 https://doi.org/10.1016/j.vetpar.2015.02.003	journal	April 2015
Distribution of platinum and other traffic related metals in sediments and clams (Corbicula sp.) Ruchter, Nadine; Sures, Bernd Water Research, Vol. 70 https://doi.org/10.1016/j.watres.2014.12.011	journal	March 2015
Strong Delayed Interactive Effects of Metal Exposure and Warming: Latitude-Dependent Synergisms Persist Across Metamorphosis Debecker, Sara; Dinh, Khuong V.; Stoks, Robby Environmental Science & Technology, Vol. 51, Issue 4 https://doi.org/10.1021/acs.est.6b04989	journal	February 2017
Metamorphosis Affects Metal Concentrations and Isotopic Signatures in a Mayfly ( Baetis tricaudatus ): Implications for the Aquatic-Terrestrial Transfer of Metals Wesner, Jeff S.; Walters, David M.; Schmidt, Travis S. Environmental Science & Technology, Vol. 51, Issue 4 https://doi.org/10.1021/acs.est.6b05471	journal	February 2017
Life Cycle Responses of the Midge Chironomus riparius to Compounds with Different Modes of Action Marinković, Marino; Verweij, Rudo A.; Nummerdor, Grietje A. Environmental Science & Technology, Vol. 45, Issue 4 https://doi.org/10.1021/es102904y	journal	February 2011
Mercury as a Global Pollutant: Sources, Pathways, and Effects Driscoll, Charles T.; Mason, Robert P.; Chan, Hing Man Environmental Science & Technology, Vol. 47, Issue 10 https://doi.org/10.1021/es305071v	journal	May 2013
Metamorphosis Alters Contaminants and Chemical Tracers in Insects: Implications for Food Webs Kraus, Johanna M.; Walters, David M.; Wesner, Jeff S. Environmental Science & Technology, Vol. 48, Issue 18 https://doi.org/10.1021/es502970b	journal	August 2014
Filarial infection influences mosquito behaviour and fecundity Gleave, Katherine; Cook, Darren; Taylor, Mark J. Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep36319	journal	October 2016
Reactive oxygen species generation by copper(II) oxide nanoparticles determined by DNA damage assays and EPR spectroscopy Angelé-Martínez, Carlos; Nguyen, Khanh Van T.; Ameer, Fathima S. Nanotoxicology, Vol. 11, Issue 2 https://doi.org/10.1080/17435390.2017.1293750	journal	February 2017
Inorganics and Hormesis Calabrese, Edward J.; Baldwin, Linda A. Critical Reviews in Toxicology, Vol. 33, Issue 3-4 https://doi.org/10.1080/713611040	journal	January 2003
Contaminants in linked aquatic–terrestrial ecosystems: Predicting effects of aquatic pollution on adult aquatic insects and terrestrial insectivores Kraus, Johanna M. Freshwater Science, Vol. 38, Issue 4 https://doi.org/10.1086/705997	journal	December 2019
Socio-Ecological Mechanisms Supporting High Densities of Aedes albopictus (Diptera: Culicidae) in Baltimore, MD Little, E.; Biehler, D.; Leisnham, P. T. Journal of Medical Entomology, Vol. 54, Issue 5 https://doi.org/10.1093/jme/tjx103	journal	June 2017
Comparative Susceptibility of Four Strains of Aedes Aegypti (Diptera: Culicidae) to Infection with Dirofilaria Immitis Buxton, Bonnie A.; Mullen, Gary R. Journal of Medical Entomology, Vol. 18, Issue 5 https://doi.org/10.1093/jmedent/18.5.434	journal	September 1981
Tangled webs: reciprocal flows of invertebrate prey link streams and riparian zones: Prey subsidies link stream and riparian food webs Baxter, Colden V.; Fausch, Kurt D.; Carl Saunders, W. Freshwater Biology, Vol. 50, Issue 2 https://doi.org/10.1111/j.1365-2427.2004.01328.x	journal	January 2005
Unusual productivity of Aedes aegypti in septic tanks and its implications for dengue control Barrera, R.; Amador, M.; Diaz, A. Medical and Veterinary Entomology, Vol. 22, Issue 1 https://doi.org/10.1111/j.1365-2915.2008.00720.x	journal	March 2008
Biological cost of tolerance to heavy metals in the mosquito Anopheles gambiae Mireji, P. O.; Keating, J.; Hassanali, A. Medical and Veterinary Entomology, Vol. 24, Issue 2 https://doi.org/10.1111/j.1365-2915.2010.00863.x	journal	March 2010
Sublethal metal stress response of larvae of Aedes aegypti: Metal stress in A. aegypti Perez, Mario H.; Noriega, Fernando G. Physiological Entomology, Vol. 39, Issue 2 https://doi.org/10.1111/phen.12054	journal	April 2014
Interactions between parasites and pollutants in yellow perch (Perca flavescens) in the St. Lawrence River, Canada: implications for resistance and tolerance to parasites Marcogliese, David J.; Dautremepuits, Claire; Gendron, Andrée D. Canadian Journal of Zoology, Vol. 88, Issue 3 https://doi.org/10.1139/Z09-140	journal	March 2010
Zika, Chikungunya, and Other Emerging Vector-Borne Viral Diseases Weaver, Scott C.; Charlier, Caroline; Vasilakis, Nikos Annual Review of Medicine, Vol. 69, Issue 1 https://doi.org/10.1146/annurev-med-050715-105122	journal	January 2018
Ecology of Insects in Urban Environments Frankie, G. W.; Ehler, L. E. Annual Review of Entomology, Vol. 23, Issue 1 https://doi.org/10.1146/annurev.en.23.010178.002055	journal	January 1978
Feeding Behavior, Natural Food, and Nutritional Relationships of Larval Mosquitoes Merritt, R. W.; Dadd, R. H.; Walker, E. D. Annual Review of Entomology, Vol. 37, Issue 1 https://doi.org/10.1146/annurev.en.37.010192.002025	journal	January 1992
Multimodel Inference: Understanding AIC and BIC in Model Selection Burnham, Kenneth P.; Anderson, David R. Sociological Methods & Research, Vol. 33, Issue 2 https://doi.org/10.1177/0049124104268644	journal	November 2004
Integrating vector control across diseases Golding, Nick; Wilson, Anne L.; Moyes, Catherine L. BMC Medicine, Vol. 13, Issue 1 https://doi.org/10.1186/s12916-015-0491-4	journal	October 2015
Parasite responses to pollution: what we know and where we go in ‘Environmental Parasitology’ Sures, Bernd; Nachev, Milen; Selbach, Christian Parasites & Vectors, Vol. 10, Issue 1 https://doi.org/10.1186/s13071-017-2001-3	journal	February 2017
Understanding trophic interactions in host-parasite associations using stable isotopes of carbon and nitrogen Nachev, Milen; Jochmann, Maik A.; Walter, Friederike Parasites & Vectors, Vol. 10, Issue 1 https://doi.org/10.1186/s13071-017-2030-y	journal	February 2017
Suppression of Laccase 2 severely impairs cuticle tanning and pathogen resistance during the pupal metamorphosis of Anopheles sinensis (Diptera: Culicidae) Du, Ming-Hui; Yan, Zheng-Wen; Hao, You-Jin Parasites & Vectors, Vol. 10, Issue 1 https://doi.org/10.1186/s13071-017-2118-4	journal	April 2017
The NIH-NIAID Filariasis Research Reagent Resource Center Michalski, Michelle L.; Griffiths, Kathryn G.; Williams, Steven A. PLoS Neglected Tropical Diseases, Vol. 5, Issue 11 https://doi.org/10.1371/journal.pntd.0001261	journal	November 2011
The effect of metal pollution on the life history and insecticide resistance phenotype of the major malaria vector Anopheles arabiensis (Diptera: Culicidae) Oliver, Shüné V.; Brooke, Basil D. PLOS ONE, Vol. 13, Issue 2 https://doi.org/10.1371/journal.pone.0192551	journal	February 2018
Suppression of Brugia malayi (sub-periodic) larval development in Aedes aegypti (Liverpool strain) fed on blood of animals immunized with microfilariae Athisaya Mary, K.; Paily, Kp; Hoti, Sl Memórias do Instituto Oswaldo Cruz, Vol. 100, Issue 4 https://doi.org/10.1590/S0074-02762005000400011	journal	July 2005
Laboratory and Field Evaluation of Metallic Copper on Aedes albopictus (Diptera: Culicidae) Larval Development Romi, Roberto; Di Luca, Marco; Raineri, Walter Journal of Medical Entomology, Vol. 37, Issue 2 https://doi.org/10.1603/0022-2585-37.2.281	journal	March 2000
Macroinvertebrate Production and food web Energetics in an Industrially Contaminated Stream Runck, Clay Ecological Applications, Vol. 17, Issue 3 https://doi.org/10.1890/05-1026	journal	April 2007
The dark side of Subsidies: Adult Stream Insects Export Organic Contaminants to Riparian Predators Walters, David M.; Fritz, Ken M.; Otter, Ryan R. Ecological Applications, Vol. 18, Issue 8 https://doi.org/10.1890/08-0354.1	journal	December 2008
Cross-ecosystem impacts of stream pollution reduce resource and contaminant flux to riparian food webs Kraus, Johanna M.; Schmidt, Travis S.; Walters, David M. Ecological Applications, Vol. 24, Issue 2 https://doi.org/10.1890/13-0252.1	journal	March 2014
Growth and secondary production of aquatic insects along a gradient of Zn contamination in Rocky Mountain streams Carlisle, Daren M.; Clements, William H. Journal of the North American Benthological Society, Vol. 22, Issue 4 https://doi.org/10.2307/1468355	journal	December 2003
Copper: Its Occurrence and Role in Insects and Other Animals Muttkowski, Richard A. Transactions of the American Microscopical Society, Vol. 40, Issue 3 https://doi.org/10.2307/3221584	journal	July 1921
Insect prophenoloxidase: the view beyond immunity Lu, Anrui; Zhang, Qiaoli; Zhang, Jie Frontiers in Physiology, Vol. 5 https://doi.org/10.3389/fphys.2014.00252	journal	July 2014
Critical Analysis of the Melanogenic Pathway in Insects and Higher Animals Sugumaran, Manickam; Barek, Hanine International Journal of Molecular Sciences, Vol. 17, Issue 10 https://doi.org/10.3390/ijms17101753	journal	October 2016
Mosquito Oviposition Behavior and Vector Control Day, Jonathan Insects, Vol. 7, Issue 4 https://doi.org/10.3390/insects7040065	journal	November 2016
Suggestions concerning an Index of Experimental Filaria Infection in Mosquitoes 1 Kartman, Leo The American Journal of Tropical Medicine and Hygiene, Vol. 3, Issue 2 https://doi.org/10.4269/ajtmh.1954.3.329	journal	March 1954
Isolation of Zika Virus from Aedes Aegypti Mosquitoes in Malaysia * Garcia, R.; Marchette, N. J.; Rudnick, A. The American Journal of Tropical Medicine and Hygiene, Vol. 18, Issue 3 https://doi.org/10.4269/ajtmh.1969.18.411	journal	May 1969

Similar Records

Drug Resistance in Filarial Parasites Does Not Affect Mosquito Vectorial Capacity

Journal Article · Mon Dec 21 19:00:00 EST 2020 · Pathogens · OSTI ID:1848978

Effects of PFOS on the behavior, growth, emergence, and predation susceptibility of larval mosquitoes (Culex quinquefasciatus)

Journal Article · Tue Dec 02 19:00:00 EST 2025 · Current Research in Insect Science · OSTI ID:3010613

Related Subjects

54 ENVIRONMENTAL SCIENCES
Aedes aegypti
Copper
Dirofilaria immitis
Environmental Sciences & Ecology
Vector competence
Vectorial capacity

The direct and indirect effects of copper on vector-borne disease dynamics

Citation Formats

References (82)

Similar Records

Related Subjects