Progress 10/01/12 to 09/30/13
Outputs
Target Audience: Ecologists, conservationists, evolutionary biologists, public health specialists, and mosquito control personnel represent important components of the audience of this report. Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided? Activities: The PI was the major advisor during this period of three PhD students, overseeing their research, reporting, examinations, publications, and support mechanisms. He additionally furthered the training of a Brazilian PhD student who conducted research for six months in our laboratories. Membership on two other Graduate Committees advanced the careers of other PhD candidates. One postdoctoral fellow worked closely with the PI on satyrization related to invasions, and former postdocs and graduate students continued to collaborate towards publication of research relevant to this project. Events: Our lab’s graduate students and postdoctoral fellow presented results of their research at annual meetings of the Ecological Society of America (Minneapolis MN), the Entomological Society of America (Austin TX), and the Florida Mosquito Control Association (Coral Springs FL), as well as at the International Congress of Vector Ecology (La Quinta CA). The same three PhD students received fellowship awards from the FMCA, the Nan-Yao Su Foundation, Monsanto, and Colciencias (Colombia) and one travel grant award from the University of Florida. The PI delivered invited presentations at a mosquito biocontrol workshop (Leipzig, Germany) and in symposia at the aforementioned Vector Ecology Congress and Entomological Society meetings. He also served the research community by participating in an ad hoc grant review panel for NIAID and served the public with various media interviews. How have the results been disseminated to communities of interest?
Nothing Reported
What do you plan to do during the next reporting period to accomplish the goals?
Nothing Reported
Impacts
What was accomplished under these goals?
Our report on resistance to satyrization (a form of reproductive interference) in Florida populations of A. aegypti sympatric with A. albopictus, published in PNAS, was a major milestone because it (a) corroborated the hypothesized importance of reproductive interference in population displacements of A. aegypti; (b) showed that evolution in the form of reproductive character displacement is in progress where these two species overlap; (c) suggested that A. aegypti has the capacity to overcome the displacement mechanism that reduced its range in the southeastern USA 25 years ago. Later in 2013 we published a follow-up paper that demonstrated satyrization susceptibility among A. aegypti from Arizona, as well as Florida, and showed that resistance to satyrization evolved rapidly in cages of allopatric A. aegypti exposed to interspecific mating by A. albopictus for multiple generations; however, achievement of the resistant phenotype exacts serious fitness costs among exposed A. aegypti. A laboratory study on the behavior of A. aegypti females injected with male accessory gland homogenates from A. albopictus showed that physiological effects of cross-mating include decreased locomotor activity as well as refractoriness to mating in injected females. These results are consistent with our hypothesis that satyrization is the primary proximal displacement mechanism of A. aegypti by A. albopictus. Our project additionally completed and submitted a review, to be published in Spanish, on the ecology of A. aegypti and A. albopictus in the Americas, with special emphasis on competitive interactions between these two species that may be associated with displacements as well as their public health threats. Following the 2009-2010 dengue outbreak in Key West, we published results from a pilot study that showed dengue virus from Florida could be vertically transmitted by both A. aegypti and A. albopictus, which mechanism may be significant for local maintenance of this arboviral pathogen between outbreaks. We tested models of growth and development on larvae of Corethrella appendiculata, which species is significant to the current project because of its selective predation on larvae of invasive mosquito prey. Empirical results fit to models showed that fourth instar larvae of this frog-biting midge species exhibit a canalized pupation threshold followed by a lengthy, canalized post-threshold period. Lastly among summaries of refereed papers, through a collaboration with molecular biologists at NIH, we described the salivary gland transcriptome (= sialome) of this species, the first known from a frog-biting midge. Novel protein families were described from C. appendiculata, as well as sequences from Wolbachia and several viruses. In a “white paper” to be published through NIH for review panels and institutional review boards, the use of mark-recapture methods, with emphasis on invasive mosquitoes, was reviewed.
Publications
- Type:
Journal Articles
Status:
Published
Year Published:
2013
Citation:
Bargielowski I, LP Lounibos & MC Carrasquilla. Evolution of resistance to satyrization: evidence of reproductive character displacement in populations of invasive dengue vectors. Proceedings of the National Academy of Sciences 110: 2888-2892.
- Type:
Journal Articles
Status:
Published
Year Published:
2013
Citation:
Bargielowski I, & LP Lounibos Rapid selection in the dengue vector Aedes aegypti in response to satyrization by invasive Aedes albopictus. Evolutionary Ecology.DOI 10.1007/s10682-013-9669-4
- Type:
Journal Articles
Status:
Published
Year Published:
2013
Citation:
Blosser EM, N Nishimura & LP Lounibos. Testing developmental plasticity in aquatic larvae of Corethrella appendiculata (Diptera: Corethrellidae). Annals Entomological Society of America 106: 810-817.
- Type:
Journal Articles
Status:
Published
Year Published:
2013
Citation:
Buckner EA, LP Lounibos & BW Alto. Vector competence and vertical transmission of Key West dengue-1 virus by Aedes aegypti and Aedes albopictus (Diptera: Culicidae) mosquitoes from Florida. Journal of Medical Entomology 50: 1291-1297
- Type:
Journal Articles
Status:
Published
Year Published:
2014
Citation:
Ribeiro JMC , Chagas AC, Pham VM, Lounibos LP, & Calvo E. An insight into the sialome of the frog biting fly, Corethrella appendiculata. Insect Molecular Biology and Biochemistry 44: 23-32
- Type:
Journal Articles
Status:
Awaiting Publication
Year Published:
2013
Citation:
Lima-Camara TN, Code�o CT, Hon�rio NA, Bruno RV4, Peixoto AA, Lounibos LP Male accessory gland substances from Aedes albopictus affect the locomotor activity of Ae. aegypti females. Memorias do Instituto Oswaldo Cruz
- Type:
Conference Papers and Presentations
Status:
Awaiting Publication
Year Published:
2013
Citation:
Rey JR & LP Lounibos. La Ecologia de Aedes aegypti y Aedes albopictus en America. In (R. Barrera, ed.) Proceedings of the II International Congress on Control of Aedes aegypti, Panamerican Health Organization, Washington, DC
- Type:
Other
Status:
Awaiting Publication
Year Published:
2014
Citation:
Lounibos LP & JD Charlwood. Mark-release-recapture in mosquito research. In: (MQ Benedict, ed.) Field Techniques in Vector Biology Research, National Institutes of Health, Bethesda MD.
|
Progress 10/01/06 to 09/30/13
Outputs
Target Audience:
Nothing Reported
Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided? Activities under this heading were supported by five grant awards, four federal (NSF & NIH) and one state (FDACS). These awards supported research that directly trained three Masters, five PhD, and two postdoctoral students at the University of Florida. Additionally, other graduate students, whose dissertations were related to this project, were served by participation of the PI on their graduate committees at the University of Central Florida (Orlando FL) and the Oswaldo Cruz Institute (Rio de Janeiro, Brazil). Professional development included participation by the PI in four international meetings and presentations related to this CRIS at 15 national venues and eight in Florida. This project and training of the scientific community were also served by contributions of the PI on nine study section (=grant review panels) meetings for NIH. How have the results been disseminated to communities of interest? Results were disseminated through (1) publications in refereed journals; (2) publications for the general public and media interviews; (3) presentations at scientific meetings and academic institutions; (4) presentations at public forums; (5) teaching and training of younger scientists. What do you plan to do during the next reporting period to accomplish the goals?
Nothing Reported
Impacts
What was accomplished under these goals?
The majority of studies that yielded refereed publications focused on aspects of larval competition, originally presumed to be the mechanism underlying displacements of Aedes aegypti by Aedes albopictus. Nine papers defined impacts of larval nutrients and their allochthonous sources, and five described interactions between larval competition and predation. Metacommunity dynamics, geographic variation in competitive abilities, and sex ratio distortion among hatching larvae were topics of other research involving the dynamics of aquatic immature stages. Five papers considered effects of the larval environment on susceptibility to, and dissemination of, chikungunya and dengue viruses by the two vector species. A global risk map for the introduction and establishment of A. albopictus was provided. Interspecific mating by A. albopictus in nature and its asymmetric effects on A. aegypti were described for the first time, opening new vistas for a role of satyrization in competitive displacement. Follow-up papers described the evolution of satyrization resistance in natural populations and their fitness consequences for A. aegypti. Two papers described, at different scales, adult habitat preferences for the two species in Florida. Outcomes of larval competition by Aedes japonicus were described in two other papers, and one publication described the dispersal behavior of the major West Nile vector, Culex pipiens.
Publications
- Type:
Journal Articles
Status:
Published
Year Published:
2013
Citation:
Bargielowski I., L.P. Lounibos and M.C. Carrasquilla. 2013. Evolution of resistance to satyrization: evidence of reproductive character displacement in populations of invasive dengue vectors. Proceedings of the National Academy of Sciences 110: 2888-2892
Bargielowski I., and L.P. Lounibos 2014. Rapid selection in the dengue vector Aedes aegypti in response to satyrization by invasive Aedes albopictus. Evolutionary Ecology.28: 193-203 (published online in 2013)
Blosser E.M., N. Nishimura and L.P. Lounibos. 2013. Testing developmental plasticity in aquatic larvae of Corethrella appendiculata (Diptera: Corethrellidae). Annals Entomological Society of America 106: 810-817
Buckner E.A., L.P. Lounibos and B.W. Alto. 2013. Vector competence and vertical transmission of Key West dengue-1 virus by Aedes aegypti and Aedes albopictus (Diptera: Culicidae) mosquitoes from Florida. Journal of Medical Entomology 50: 1291-1297
Lima-Camara T.N., C. Torres Code�o, N.A. Hon�rio, R. Vieira Bruno, A.A. Peixoto,and L.P. Lounibos LP.2013. Male accessory gland substances from Aedes albopictus affect the locomotor activity of Aedes aegypti females. Memorias do Instituto Oswaldo Cruz 108 (Suppl. I): 18-25
Ribeiro J.M.C., A.C. Chagas, V.M. Pham, L.P. Lounibos, and E. Calvo. 2014. An insight into the sialome of the frog biting fly, Corethrella appendiculata. Insect Molecular Biology and Biochemistry 44: 23-32 (published online in 2013)
|
Progress 10/01/11 to 09/30/12
Outputs
OUTPUTS: Activities. During the reporting period I was the major advisor to three PhD students, overseeing their examinations, research, reporting, and graduate support. I further served on thesis committees for three other PhD students, including one who defended her dissertation in March 2012 on Aedes albopictus expansion models. I also advised one postdoctoral fellow and worked with several former postdocs and graduate students to publish their research in refereed journals. Research plans focused on reproductive interference and larval competition, two putative mechanisms of post-invasion patterns observed among our mosquito species. These topics carried over to collaborative projects in Rio de Janeiro, Brazil, where I visited with colleagues at FIOCRUZ for one week in November 2011 to plan reports and publications. In two independent entomology classes for University of Florida students, I lectured on biological control, mosquito ecology, and malaria. Routinely, I performed field collections with students, including a week-long trip to Texas, and in June 2012 received a UF/IFAS award for an outstanding research publication. Events. Three relevant presentations, two talks and a poster, on invasive Aedes were delivered in November 2011 by myself and students at the annual FMCA meeting in Jacksonville. Invited seminars on related themes were presented in May 2012 to NIH/NIAID research labs in Rockville, Maryland and in August 2012 at a U.S.-Brazil Vector Symposium at NIAID's Rocky Mountain Laboratory in Hamilton, Montana. In September 2012 I delivered a keynote address on A. albopictus invasions at Surfer's Paradise, Queensland to the Mosquito Control Association of Australia. Co-authored posters, featuring results from invasive Aedes research in Rio de Janeiro, were presented in August 2012 at the annual meeting of the Ecological Society of America in Portland, Oregon, and in September 2012 at the Third Pan-American Dengue Research Network Meeting in Cartagena, Colombia. Service. As a charter member of NIAID's Vector Biology Study Section, I reviewed grant proposals and participated in two meetings to prioritize, based on scientific merit, their suitability for federal funding; one meeting was in Bethesda, Maryland in October 2011, and the other was conducted by Internet Assisted Review in June 2012. Throughout the period of this report, I served public interests with media interviews, especially about the controversial proposed releases of GM mosquitoes to control A. aegypti in the Florida Keys. PARTICIPANTS: Nothing significant to report during this reporting period. TARGET AUDIENCES: Nothing significant to report during this reporting period. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.
Impacts
The first paper published during this period described adaptive changes in diapause responses by Aedes albopictus in the southeastern USA, and the protectiveness of diapause against weather-related mortality. Other research demonstrated that A. albopictus and A. aegypti from Florida are excellent vectors of DEN1 virus, isolated from the Florida Keys, both horizontally and vertically. Intensive sampling of the container mosquito community in the Washington, DC area showed a significant negative association between the two invasive species, Aedes japonicus and A. albopictus, but concomitant and subsequent adult trapping indicated no declines in native mosquito species of this community. Mark-release-recapture experiments were used to assess survivorship of the invasive West Nile virus vector Culex pipiens in the Washington, DC area. Daily survival was estimated as 0.904 and was negatively affected by rainfall. Reserve-dependent growth of invasive A. aegypti was modeled between 20-30 degrees C, relating energy flows and providing frameworks for analyzing how climate change, density dependence, and human behaviors may alter population dynamics and disease risks associated with this vector species. Basal larval resources, as leaf species combinations, were examined for their effects on production of A. aegypti and A. albopictus. Leaf combinations were generally synergistic and non-additive, although a few combinations were antagonistic for A. albopictus. Spatial and temporal patterns of abundance of these same two species were examined on replicated transects of landscape, extending from the coast to 20 km inland in Palm Beach County, Florida. Aedes aegypti predominated in the drier habitats closer to the coast while A. albopictus was more abundant in the wetter, inland habitats. During a dengue epidemic in Rio de Janeiro, we tested individual, wild-caught females for dengue infection status and measured wing lengths as an index of competitive stress; a significant positive relationship between body size and probability of infection did not support the hypothesized relationship between competition and susceptibility to infection. Allopatric and sympatric A. aegypti strains from Florida were compared for their susceptibility to interspecific mating by A. albopictus. As predicted, A. aegypti females from populations sympatric to A. albopictus were significantly more resistant to cross-insemination, demonstrating rapid sexual selection for reproductive character displacement.
Publications
- Alto BW & LP Lounibos. 2012. Vector competence for arboviruses in relation to the larval environment of mosquitoes.Pp. 80-101 IN: (S Koenraadt & W Takken, eds.) Ecology of Vector-parasite Interactions, Wageningen Academic, The Netherlands.
- Armistead JS, N Nishimura, JR Arias & LP Lounibos. 2012. Community ecology of container mosquitoes (Diptera: Culicidae) in Virginia following invasion by Aedes japonicus. Journal of Medical Entomology 49: 1318-1327.
- Jones CJ, LP Lounibos, P Marra & AM Kilpatrick. 2012. Survival of Culex pipiens mosquitoes in a residential environment in the mid-Atlantic, USA. Journal of Medical Entomology 49: 467-473.
- Lounibos L.P., R.L. Escher and N. Nishimura. 2011. Retention and adaptiveness of photoperiodic egg diapause in Florida populations of invasive Aedes albopictus (Skuse). Journal of the American Mosquito Control Association 27: 433-436.
- Reiskind MH & LP Lounibos. 2012. Spatial and Temporal Patterns of Abundance of Aedes aegypti and Aedes albopictus in southern Florida. Medical and Veterinary Entomology (in press).
- Reiskind MH, AA Zarrabi & LP Lounibos. 2012 Effects of combinations of leaf resources on competition in container mosquito larvae. Bulletin of Entomological Research 102: 424-434.
- Rey JR & LP Lounibos. 2012 . El dengue en Latinoamerica. Investigacion y Ciencia (Madrid). 424 (Enero): 13-14.
- Padmanabha H, F Correa, M Legros, HF Nijhout, C Lord & LP Lounibos. 2012. An eco-physiological model of the impact of temperature on Aedes aegypti life history traits. Journal of Insect Physiology dx.doi.org/10.1016/j.jinsphy.2012.09.015
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Progress 10/01/10 to 09/30/11
Outputs
OUTPUTS: Research results were disseminated through international, national, regional, and local meetings and presentations. In September 2011 a symposium address was delivered (in Spanish) in Bogota, Colombia on invasive dengue vectors at the 20th Latin American Congress of Parasitology and 15th Colombian Congress of Parasitology and Tropical Medicine. In December 2010 recent results on reproductive competition in mosquitoes were presented at the annual meeting of the Entomological Society of America in San Diego. Two invited lectures in November 2010 at the University of Notre Dame highlighted results from this project, the first a George B. Craig Memorial Lecture to the Department of Biology, and the second a colloquium to the Eck Institute of Global Health. On the regional front, an illustrated lecture on asymmetric reproductive interference in invasive Florida Aedes spp. was delivered to the annual meeting of the Florida Mosquito Control Association in the Florida Keys in November 2010. Appropriately modified research presentations were also delivered to IFAS Deans at the Florida Medical Entomology Lab in June 2011 and to the Ft. Pierce Rotary Club in March 2011. Less formally, results were also shared and divulged during my participation in NIH/NIAID's Vector Biology Study Section, which met three times during this reporting period (October 2010, February 2011, June 2011). Three PhD students and one postdoctoral fellow have participated in, and contributed to, this research supported by two NIH (R21 and R01) grants on invasive vectors. Additionally, a smaller NIH (R03) grant has transported this research to Brazil, where two co-investigators, three recent PhDs, and three graduate students have used offshoots of this project for their investigations at the Oswaldo Cruz Institute in Rio de Janeiro. PARTICIPANTS: Nothing significant to report during this reporting period. TARGET AUDIENCES: Nothing significant to report during this reporting period. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.
Impacts
We measured the strength of diapause responses from six populations of invasive A. albopictus collected in 2008 from the U.S.A. In response to short daylengths, populations from Missouri to northern Florida diapaused uniformly, but the responses of southern Florida offspring were polymorphic, with two of three populations showing an increased mean incidence of diapause compared to estimates made ten years earlier. Outdoor exposures during Vero Beach winter demonstrated enhanced survivorship of short day eggs, believed to be attributable to their superior desiccation resistance compared to long day counterparts. A review article on the increasing impact of A. albopictus suggested that this species should be considered as a public health risk for dengue transmission. Analyses of nutrient contents in cemetery vases containing the immature stages of invasive mosquitoes showed that nutrient abundances were strong predictors of the relative abundance of A. aegypti. Detritus inputs, and nutrient and food availability in vases seem to contribute to the distributions of invasive Aedes spp. in cemeteries by regulating the intensity of interspecific competition. In a separate but related study, detrital diversity, as measured by leaf species falling into containers, was related to the outcomes of intra- and interspecific competition in A. aegypti and A. albopictus. Results demonstrated that combinations of leaves increased mosquito production non-additively and acted synergistically to produce higher mosquito yields. Mark-release-recapture (MRR) experiments were performed in the suburbs of Washington, D.C. with females of the invasive vector of West Nile virus, Culex pipiens. Daily survivorship did not differ between two years of MRR and was negatively affected by rainfall. WNV transmission by this vector species is reaffirmed as predominantly local by limited evidence for dispersal of this species. Laboratory experiments demonstrated complex and stage-specific relationships between starvation resistance and temperature among invasive A. aegypti. We also described how rearing temperature and larval food affect allometric scaling between wing size and epidermal cell size in individuals of this species. Reduced temperature and increased larval food produced longer wings, but only temperature affected cell size. Both studies underscored the importance of interactions between temperature and food conditions for larval growth. Interspecific mating between A. albopictus and A. aegypti was documented for the first time in nature, by the application of species-specific DNA probes to sperm dissected from the spermathecae of wild caught females. While evidence of bidirectional interspecific mating was obtained from samples from two auto salvage yards in southern Florida, complementary laboratory experiments demonstrated an asymmetric effect of male accessory gland substances transferred between species. The uni-directional sterilization of A. aegypti females by accessory gland proteins of A. albopictus revives the concept of satyrization as a mechanism to explain observed competitive displacements of A. aegypti by A. albopictus in nature.
Publications
- Rey JR & LP Lounibos. 2012. El dengue en Latinoamerica. Investigacion y Ciencia (Madrid).
- Lounibos L.P. 2011. Eco-epidemiologia del dengue: relevancia de dos vectores invasores. Biomedica 31 (Suppl.3): 57-59.
- Lounibos L.P., R.L. Escher & N. Nishimura. 2011. Retention and adaptiveness of photoperiodic egg diapause in Florida populations of invasive Aedes albopictus (Skuse). Journal of the American Mosquito Control Association 27: 433-436.
- Murrell EB, K Damal, SA Juliano & LP Lounibos. 2011. Distributions of aquatic insects depend on detritus types, nutrient ratios, and food availability. Annals of the Entomological Society of America 104:688-698.
- Padmanabha H., B. Bolker, C.C. Lord, C. Rubio & L.P. Lounibos. 2011. Food availability alters the effects of larval temperature on Aedes aegypti growth. Journal of Medical Entomology 48: 974-984.
- Padmanabha H, CC Lord & LP Lounibos. 2011. Interactive effects of temperature and instar on starvation resistance in Aedes aegypti (L.) larvae. Medical and Veterinary Entomology 25: 445-453.
- Tripet F, LP Lounibos, D Robbins, J Moran, N. Nishimura & E Blosser. 2011 Competitive reduction by satyrization Evidence for interspecific mating in nature and asymmetric reproductive competition between invasive mosquito vectors. American Journal of Tropical Medicine and Hygiene 85:265-270.
- Alto BW & LP Lounibos. 2012. Vector competence for arboviruses in relation to the larval environment of mosquitoes. IN: (S Koenraadt & W Takken, eds.) Ecology of Vector-parasite Interactions, Wageningen Academic, The Netherlands.
- Jones CJ, LP Lounibos, P Marra & AM Kilpatrick. 2012. Survival of Culex pipiens mosquitoes in a residential environment in the mid-Atlantic, USA. Journal of Medical Entomology.
- Reiskind MH, AA Zarrabi & LP Lounibos. 2012. Effects of combinations of leaf resources on competition in container mosquito larvae. Bulletin of Entomological Research.
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Progress 10/01/09 to 09/30/10
Outputs
OUTPUTS: Site visits to Bogota, Cali, and Barranquilla facilitated development with Colombian colleagues of two federal grant applications, one on human ecology and urban dengue, the other on reproductive interference and competitive displacement. Supervision and review was also supplied to research colleagues in Rio de Janeiro who are supported by our NIH grant entitled Invasive Aedes and Dengue in Brazil. Two University of Florida (UF) Ph.D students and one MSc. student successfully defended their dissertations and completed their degrees, which will culminate in multiple publications in refereed journals. Ph.D. qualifying examinations were completed by two additional UF students, one in the Department of Entomology and the other in Biology. Two other Ph.D students began their training and coursework in Gainesville, and a summer intern from Johns Hopkins University learned mosquito biology techniques at our laboratory in Vero Beach. Three invited seminars were presented at two institutions, the University of Texas Medical Branch and the University of Notre Dame, the latter including the Craig Memorial Lecture, which honors the memory of the late doyen of mosquito biology in the USA. I organized a symposium on mosquito ecology and arbovirus transmission for the annual meeting of the Florida Entomological Society and presented updates on research on reproductive competition in this venue, as well as at the annual meetings of the Florida Mosquito Control Association and Entomological Society of America. Course lectures were delivered to public health students at the University of South Florida (USF) (malaria vectors) and to UF graduate students (mosquito biocontrol and advanced mosquito biology). The scientific merit of approximately one hundred research proposals submitted to NIH was critiqued at two meetings of the Vector Biology Study Section. Among published products, results were disseminated in a trade journal (Wing Beats) article, two book chapters, and seven papers in refereed journals. Grant proposals to NIH were submitted as co-PI (UF/USF consortium) and PI (UF/FMEL). PARTICIPANTS: Nothing significant to report during this reporting period. TARGET AUDIENCES: Nothing significant to report during this reporting period. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.
Impacts
Further experiments explored mosquito-arbovirus relationships using Chikungunya, an emerging public health threat within the range of invasive mosquito species common in Florida. Longevity of Aedes albopictus, the most efficient vector of the emergent strain, was significantly decreased by CHIKV infection. Water storage and emptying behaviors were shown to regulate dengue vector production in three Colombian cities on an altitudinal gradient. Owing to different mean temperatures, which affect larval development time, the emptying intervals required to discourage pupal production differed among the cities. Relationships between microclimate and the maintenance or extinction of Aedes aegypti in south Florida cemeteries were explored through egg survivorship experiments in six cemeteries. Results were consistent with the hypothesis that Aedes albopictus, but not A. aegypti, suffers site-specific, climate-driven egg mortality that mitigates the competitive superiority of larval A. albopictus over A. aegypti. Using a newly devised molecular diagnostic probe on sperm extracted from female spermathecae, we demonstrated that A. aegypti and A. albopictus mate with one another in two south Florida salvage yards. Subsequent injections of male accessory gland (MAG) homogenates into virgin females of the two species revealed that A. albopictus MAGs sterilize female A. aegypti, but A. aegypti MAGs do not affect female A. albopictus. Owing to the consequent asymmetry of MAG effects, satyrization is now believed to have played a major role in the competitive displacement of A. aegypti by A. albopictus in the southeastern USA and elsewhere, such as Bermuda.
Publications
- Lounibos LP. 2010. Mosquitoes. Pp.462-466 In (D. Simberloff & M. Rejmanek, eds.) Encyclopedia of Invasive Species, University of California Press, Berkeley.
- Lounibos LP & SA Juliano. 2010. Worst enemy or best friend Wing Beats 21:33-34.
- Lounibos LP, GF OMeara, SA Juliano, N Nishimura, RL Escher, MH Reiskind, M Cutwa & K Greene. 2010. Differential survivorship of invasive mosquito species in south Florida cemeteries: do site-specific microclimates explain patterns of coexistence and exclusion Annals of the Entomological Society of America 103: 757-770.
- Juliano SA, LP Lounibos, N Nishimura & K Greene. 2010. Your worst enemy could be your best friend: predator contributions to invasion resistance and persistence of natives. Oecologia 162: 709-718
- Lounibos LP. 2010. Human Disease Vectors. Pp. 150-154 In (D. Simberloff & M. Rejmanek, eds.) Encyclopedia of Invasive Species, University of California Press, Berkeley.
- Padmanabha H, E Soto, M Mosquera, C Lord & LP Lounibos. 2010 Ecological impact of water storage behaviors on Aedes aegypti production: implications for intervention in changing environments. Ecohealth 7:78-90.
- Reiskind MH, CJ Westbrook & LP Lounibos. 2010. Chikungunya infection and adult longevity in Aedes aegypti L. and Aedes albopictus Skuse. Journal of Vector Ecology 35:61-68.
- Reiskind MH, A Zarrabi, LP Lounibos. 2010. Invasive leaf resources alleviate density dependence in the native mosquito, Aedes albopictus. Biological Invasions 12: 2319-2328.
- Rey JR, LP Lounibos, H. Padmanabha & M Mosquera. 2010 Resurgencia del dengue en America: Pautas, procesos, y propsectos. Interciencia 35:800-806.
- Westbrook CJ, Pesko K, Reiskind MH, Greene K, Lounibos LP. 2010. Larval environmental temperature and the susceptibility of Aedes albopictus to chikungunya virus. Vector-Borne and Zoonotic Diseases 10: 241-247
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Progress 10/01/08 to 09/30/09
Outputs
OUTPUTS: This CRIS was advanced during the current reporting period by new collaborations, mentoring, conferences, symposia, training, consulting, and the production of new scientific results. New discoveries about the ecology of urban dengue in Colombia were presented at meetings and submitted for publication. American and Brazilian collaborators met in Rio de Janeiro in July to further research there on the role of larval competitors and dengue, and a Brazilian Ph.D. student completed experiments in Florida which contributed to this project. While in Rio, the PI served as external examiner during the thesis defense of project collaborator N. Honorio, who was awarded the Ph.D. from FIOCRUZ. Two graduate student committee meetings, one a thesis defense (P. Obenauer), and one a qualifying examination (K. Medley), were participated in at, respectively, the University of Florida (UF) and the University of South Florida. A new graduate student (P. Herrera) was recruited to UF while the PI consulted on the control of dengue vectors at the University of San Carlos in Guatemala. During this reporting period the PI was added to the roster of Fulbright Technical Specialists for a future foreign assignment, probably in Argentina. Project results were reported at the International Symposium on the Asian Tiger Mosquito at Rutgers, and the PI's expertise was utilized at state-supported Rift Valley Fever exercise in Tallahassee, Florida. The scientific merit of proposals submitted to NIH was evaluated at two meetings in Maryland of the Vector Biology Study Section. A lecture on Tropical Entomology was provided for graduate students in that course in Gainesville. Finally, 12 papers related to this CRIS were accepted or published by refereed journals. PARTICIPANTS: Nothing significant to report during this reporting period. TARGET AUDIENCES: Nothing significant to report during this reporting period. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.
Impacts
Research on vector-virus relationships continued, using Chikungunya, which was responsible for recent outbreaks of human disease in the Asian subcontinent and Indian Ocean regions. Although both Aedes aegypti and Aedes albopictus from Florida were susceptible to CHIKV, only the latter species disseminated infections with the lowest doses tested of this virus isolated from Reunion, and infection rates of both species were dependent on blood meal delivery system. Larval rearing temperature was found to markedly affect the infection rates of A. albopictus with CHIKV, females exposed to 18 degrees C being six times more likely to become infected than counterparts reared at 32 degrees C. The relationship between larval competition and adult longevity was examined in the aforementioned species. Negative effects of competition on survival were detected for A. aegypti but not A. albopictus. We tested the hypothesis that larval survival and growth of these two species depended upon the species of leaf fallen into containers. This hypothesis was validated, and larvae grew larger and survived better on resources of mixed-species leaves. We also reported on experiments that demonstrated that leaves of invasive species (Brazilian pepper) alleviated density dependence in larval A. albopictus. Competitive abilities of A. albopictus from nine sites in eastern USA were compared on a standardized larval resource. Results suggested that interpopulation variation in the competitive ability of this species may account, in part, for patterns of coexistence with, or exclusion of, A. aegypti. The sources of differential susceptibility of invasive and native container mosquitoes to larval predation were investigated in laboratory microcosm experiments. Prey size, in conjunction with anti-predator behaviors, altered asymmetric predation and predator-mediated coexistence. A subsequent field experiment using the same prey and predator species showed that low or moderate densities of larvae of the frog-biting midge Corethrella appendiculata prevented successful colonization of water-holding tires by the invasive A. albopictus, in the presence of the native mosquito Aedes triseriatus.
Publications
- Pesko K, CJ Westbrook, CN Mores, LP Lounibos & MH Reiskind. 2009. Effects of Infectious Virus Dose and Bloodmeal Delivery Method on Susceptibility of Aedes aegypti and Aedes albopictus to Chikungunya Virus. Journal of Medical Entomology 46: 395-399.
- Reiskind MH & LP Lounibos. 2009. Effects of intraspecific larval competition on adult longevity in the mosquitoes Aedes aegypti and Aedes albopictus. Medical and Veterinary Entomology 23:62-68.
- Alto BW, B Kesavaraju, SA Juliano & LP Lounibos. 2009. Stage-dependent predation on competitors: consequences for the outcome of a mosquito invasion. Journal of Animal Ecology 78: 928-936.
- Leisnham PT, LP Lounibos, GF OMeara & SA Juliano. 2009. Interpopulation divergence in competitive interactions of the mosquito Aedes albopictus. Ecology 90: 2405-2413.
- Westbrook CJ, MH Reiskind, KN Pesko, KL Greene & LP Lounibos. 2009. Larval Environmental Temperature and the Susceptibility of Aedes albopictus Skuse (Diptera: Culicidae) to Chikungunya Virus. Vector-borne and Zoonotic Diseases DOI: 10.1089/vbz.2009.0035.
- Juliano SA, LP Lounibos, N Nishimura & K Greene. 2009. Your worst enemy could be your best friend: predator contributions to invasion resistance and persistence of natives. Oecologia DOI 10.1007/s00442-009-1475-x.
- Reiskind MH, AA Zarrabi, & LP Lounibos.2009. Invasive leaf resources alleviate density dependence in the invasive mosquito, Aedes albopictus. 2009. Biological Invasions DOI 10.1007/s10530-009-9646-6.
- Mocellin MG, TC Simoes, TF Silva do Nascimento, MLF Teixeira , LP Lounibos & R Lourenco de Oliveira. 2009. Bromeliad-inhabiting mosquitoes in an urban botanical garden of dengue endemic Rio de Janeiro: Are bromeliads productive habitats for the invasive vectors Aedes aegypti and Aedes albopictus Memorias do Instituto Oswaldo Cruz.
- Reiskind MH, CJ Westbrook & LP Lounibos. 2010. Chikungunya Infection and Adult Longevity in Aedes aegypti L. and Aedes albopictus Skuse. Journal of Vector Ecology.
- Padmanabha H, E Soto, M Mosquera & LP Lounibos. 2010. Ecological impact of water storage behaviors on Aedes aegypti production: implications for intervention in changing environments. Ecohealth.
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Progress 10/01/07 to 09/30/08
Outputs
OUTPUTS: This CRIS was supported during the current reporting period by new experiments, mentoring, conferences, symposia, training, consulting, and scientific results. Two international projects on dengue ecology were furthered by a new NIH grant for research in Brazil and positive reviews on an NSF application for research in Colombia. The NIH/FIRCA grant supported travel to Rio de Janeiro for meetings of American and Brazilian collaborators to lay out research designs for investigations on the effects of larval competition among invasive Aedes vectors on dengue transmission. The goals of that project were also advanced by the arrival at FMEL of T. Riback, supported by a seven-month fellowship from the Brazilian government, to perform experiments on larval development of invasive Aedes in relation to temperature. Two Ph.D students supervised by this PI, H. Padmanabha and C. Westbrook, passed qualifying examinations and delivered seminars about their research on invasive Aedes. Two other students in earlier stages of their graduate studies, C. Johnson and E. Blosser, completed required courses and began formulating research programs on invasive vector mosquitoes. Two additional Ph.D. students, P. Obenauer (Univ. of Florida) and K. Medley (Univ. Central Florida) were also advised about Aedes albopictus in relation to their doctoral research, and presentations were delivered in departmental (ENY 5241) and FMEL (Mosquito Identification) courses. Presentations of project results were made in diverse contexts of the Univ. of Florida: at FMEL to HHMI undergraduates; to the Florida Vector-borne Diseases Working Group of EPI; in St. Augustine to the Climate Change Group of EPI. Outside this University, I presented results from this CRIS in May as an invited guest lecturer in the Dept. of Entomology of UC Davis; in September in a biosystematics symposium at the annual meeting of the Society of Vector Ecology; in February via a teleconference with collaborators on an NSF/EID project. Service on two NIH study sections, one in February via the internet, and the second in person in Maryland, benefitted the scientific community with interests in invasive vectors. Finally, eleven refereed papers related to this CRIS, were published or accepted for publication (see Publications). PARTICIPANTS: Not relevant to this project. TARGET AUDIENCES: Not relevant to this project. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.
Impacts
Experiments at FMEL identified the impacts of biotic and abiotic factors on vector competence of invasive Aedes for two important arboviruses. Both A. albopictus and A. aegypti from Florida were shown to be excellent vectors of chikungunya virus (CHIKV), and infection rates of A. albopictus for this virus were inversely related to larval rearing temperatures. CHIKV-infected A. albopictus, but not A. aegypti females, suffered reduced adult survivorship compared to uninfected control mosquitoes. Larval competition between and among these two species was shown to increase infection with and transmission of dengue virus (DENV). Members of this project also discovered that smaller-sized vectors were significantly more likely to become infected by and disseminate DENV than larger counterparts. Experiments conducted outdoors in northern Virginia confirmed the presence of intense interspecific competition between the two invasive species, A. albopictus and A. japonicus. Based on performances in artificial containers, A. albopictus was predicted to displace A. japonicus owing to the asymmetric outcome of interspecific interactions, which favored the former species. Simulated rock pools were used to investigate larval competition between and among the invasive species A. japonicus and A. atropalpus. In these experiments, the effects of interspecific competition were less than those of intraspecific competition, which was more severe on the autogenous species, A. atropalpus. The effects of larval competition on adult survival were investigated in laboratory experiments, which demonstrated strong negative effects on A. aegypti, but not on A. albopictus. Leaves from four species of native plants were compared as larval resource bases and oviposition stimulants for the container species A. albopictus and A. triseriatus. Larval growth and survival differed among the four leaf species, and results from leaf combination experiments rejected an additivity model. Competitive abilities of A. albopictus from different populations in the USA were shown to vary geographically, but trends were not correlated with co-occurrences of this species with A. aegypti. The role of larval competition on invasive Aedes in bromeliads was discussed in a new review article on insects of bromeliads.
Publications
- Armistead JS, JR Arias & LP Lounibos. 2008. Interspecific larval competition between Aedes albopictus and Aedes japonicus (Diptera: Culicidae) in northern Virginia. Journal of Medical Entomology 45: 629-637.
- Alto BW, LP Lounibos, CN Mores & MH Reiskind. 2008. Larval competition alters adult susceptibility to dengue infection. Proceedings of the Royal Society of London, Series B. 275: 463-471.
- Armistead JS, N Nishimura, RL Escher & LP Lounibos. 2008. Larval competition between Aedes japonicus and Aedes atropalpus in simulated rock pools. Journal of Vector Ecology 33: 238-246. Lounibos LP & RL Escher. 2008. Sex ratios of mosquitoes from long-term censuses of Florida tree holes. Journal of the American Mosquito Control Association 24: 11-15.
- Lounibos LP, S Makhni, BW Alto & B Kesavaraju. 2008. Surplus killing by predatory larvae of Corethella appendiculata: prepupal timing and site-specific attack on mosquito prey. Journal of Insect Behavior 21: 47-54.
- Reiskind MH, K Pesko, CJ Westbrook & CN Mores. 2008. Susceptibility of Florida mosquitoes to infection with chikungunya virus. American Journal of Tropical Medicine and Hygiene 78: 422-425.
- Frank JH & LP Lounibos. 2008. Insects and allies associated with bromeliads: a review. Terrestrial Arthropod Reviews 1:
- Leisnham PT, LP Lounibos, GF OMeara & SA Juliano. 2009. Geographic divergence in competitive effect and response of the mosquito Aedes albopictus and the potential role of a non-competing life-stage in its invasion success. Ecology.
- Reiskind MH, K Greene & LP Lounibos. 2009. Leaf species identity and combination affect performance and oviposition choice of two container mosquito species. Ecological Entomology.
- Reiskind MH & LP Lounibos 2009 Intraspecific competition and adult survival in Aedes aegypti and Aedes albopictus. Medical and Veterinary Entomology.
- Alto BW, MH Reiskind & LP Lounibos. 2008 Size alters susceptibility of vectors to dengue virus infection and dissemination. American Journal of Tropical Medicine and Hygiene 79: 688-695.
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Progress 10/01/06 to 09/30/07
Outputs
Two new federal grants furthered the reach of this CRIS project: (1) NSF/EID #EF-062239 "Predicting Spatial Variation in West Nile Virus Transmission" and (2) NIH/FIC #R03TW007446 "Invasive Aedes Mosquitoes and Dengue in Brazil". The former grant will support the graduate training of C. Johnson, who was accepted in June 2007 to the Master's program in entomology at the University of Florida (UF), and the latter grant unites researchers under this CRIS at UF, Illinois State University, and FIOCRUZ (Rio de Janeiro, Brazil) to assess the role of larval competition in dengue transmission in nature. New collaborations and graduate trainees were also initiated during this report period. A subcontract to Dr. F. Tripet of Keele University (UK) is facilitating research on the role of adult competition (aka satyrization) in displacement of Aedes aegypti by Aedes albopictus. In January of 2007 C. Westbrook began Ph.D. research at UF/FMEL focusing on the effects of larval
temperature on the transmission of chikungunya virus by invasive Aedes spp. For his Ph.D. thesis, H. Padmanabha is studying relationships between human ecology, the production of invasive vector mosquitoes, and dissemination of dengue virus in urban Colombia. In July of 2007 the PI delivered a plenary address (in Spanish) on the ecology of invasive mosquitoes to the annual Congress of the Entomological Society of Colombia, which met in Cartagena. After this meeting, he met in Bogota with graduate student Padmanabha and collaborators to develop plans and a grant proposal for further research on the ecology of dengue vectored by invasive Aedes spp. In October 2006 trainee R. Raban successfully defended her MSc. thesis on the ecology of invasive Aedes in Florida, and in March of 2007 J. Armistead successfully defended her MSc. thesis on interspecific competition among invasive Aedes spp. in northern Virginia. Members of our research team presented recent scientific results on invasive
mosquito ecology at the annual meetings of the: (a) American Society of Tropical Medicine and Hygiene (November 2006, Atlanta GA); (b) Entomological Society of America (December 2006, Indianapolis IN); (c) American Mosquito Control Association (April 2007, Orlando FL); (d) Ecological Society of America (August 2007, San Jose CA). Dissemination of project outputs included diverse published materials. The presentations at the aforementioned meetings all included published abstracts accessible to society members and meeting attendees. More importantly, ten papers describing recent research results from this project were either published or in press during this reporting period. Although the majority of these papers (6) are in refereed entomological journals, the readership of ecological, infectious disease and tropical medicine, and general biological journals were also exposed to our new results. Furthermore, one review paper was published in Spanish, extending the dissemination of
results to, especially, a Latin American audience.
Impacts
Long-term census records of the treehole mosquito community in south Florida, which includes Aedes albopictus, were used to evaluate predictions of four metacommunity models. Population dynamics supported a species sorting model, and turnover supported a patch dynamics model. Mass effects and neutral models were not supported by this data set. A Genetic Algorithm for Rule Set Production was used to predict a global risk map for the spread of A. albopictus. This methodology may be valuable for predicting risks from future invasions of vectors or pathogens. Invasive arbovirus vectors were collected by ovitraps in diverse habitats across south Florida. Subsequently, aerial images of these habitats were obtained, digitized, and codified by dummy variables. Multiple regression models which incorporated the habitat variables explained significant variation in the abundances of Aedes aegypti and A, albopictus but were opposite in sign for these two species. In a laboratory
experiment designed to evaluate the effects of larval competition on vector competence, infection and dissemination of dengue virus was facilitated by intense larval competition in A. albopictus, but not A. aegypti. The similarity of responses of these two mosquito species to two unrelated viruses, dengue and Sindbis, suggests that a generalizable mechanism underlies this response to competitive stress. The role of predation in the spread of invasive mosquitoes was evaluated by experiments using Corethrella appendiculata as a predator of A. albopictus and Aedes triseriatus. Only the latter adopted low-risk behaviors in the presence of cues of this predator species, and larvae of this native mosquito responded in all four instars. Second instar larvae of both species were more vulnerable than thirds to consumption by this predator, but third-stage A. albopictus were preferred to A. triseriatus of the same instar. These results support the hypothesis that selective predation promotes
co-existence of the invasive and native mosquito species in containers. A literature review suggested that larval competition was the likely explanation of examples of competitive displacement or reduction of mosquito species by ecological homologs. Although competitive displacement may have potential for mosquito control, more ecological research is needed. Long-term records of pupae in treehole censuses showed that seasonal sex ratio biases favored males of A. triseriatus, but no overall bias was detected for A. albopictus or Toxorhynchites rutilus. These results were interpreted in the context of sexual selection and differential responses of male and female eggs of A. triseriatus to hatching stimuli. Surplus killing was identified for the first time in larvae of C. appendiculata. This behavior was detected only among prepupae, in which growth stage Toxorhynchites spp. evince similar behavior, and was associated with site-specific attacks on the thorax of mosquito prey. The
functional and evolutionary significance of surplus killing in these dipterans is unclear.
Publications
- Ellis AM, Lounibos LP & Holyoak M. 2006. Examining the long-term metacommunity dynamics of treehole mosquitoes. Ecology 87: 2582-2590.
- Rey JR, Nishimura N, Wagner B, Braks MAH, OConnell SM & Lounibos LP. 2006. Habitat segregation of mosquito arbovirus vectors in south Florida. Journal of Medical Entomology 43: 1134-1141
- Alto BW, Lounibos LP, Mores CN & Reiskind MH. 2007. Larval competition alters adult susceptibility to dengue infection. Proceedings of the Royal Society of London, Series B. Online at: DOI:10.1098/rspb.2007.1497.
- Benedict MQ, Levine RS, Hawley WA & Lounibos LP. 2007. Spread of the tiger: global risk of invasion by the mosquito Aedes albopictus. Vector-borne and Zoonotic Diseases 7: 76-85.
- Kesavaraju B, Alto BW, Lounibos LP & Juliano SA. 2007. Behavioural responses of larval container mosquitoes to a size-selective predator. Ecological Entomology 32: 262-272.
- Lounibos LP 2007. Competitive displacement and reduction. In: (TE Floore, ed) Biorational Control of Mosquitoes. Bulletin No. 7 of the American Mosquito Control Association 23 (Suppl. No.2):276-282.
- Lounibos LP & Rey JR. 2007. Ecologia de mosquitos invasores y su impacto en la salud publica. Pp. 22-28 En: Memorias de XXXIV Congreso Sociedad Colombiana de Entomologia, Cartagena.
- Lounibos LP & Escher RL. 2008. Sex ratios of mosquitoes from long-term censuses of Florida tree holes. Journal of the American Mosquito Control Association 24: (in press).
- Lounibos LP, Makhni S, Alto BW & Kesavaraju B. 2008. Surplus killing by predatory larvae of Corethella appendiculata: prepupal timing and site-specific attack on mosquito prey. J. Ins. Behav. (in press).
- Reiskind MH, K Pesko, CJ Westbrook & CN. Mores. 2008. Competence of Florida vector mosquitoes to transmit the La Reunion strain of chikungunya virus. American Journal of Tropical Medicine and Hygiene (in press).
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