Skip to main content
SpringerLink
Log in

Globally invasive, withdrawing at home: Aedes albopictus and Aedes japonicus facing the rise of Aedes flavopictus

  • Original Paper
  • Published:
International Journal of Biometeorology Aims and scope Submit manuscript

Abstract

It has been suggested that climate change may have facilitated the global expansion of invasive disease vectors, since several species have expanded their range as temperatures have warmed. Here, we present results from observations on two major global invasive mosquito vectors (Diptera: Culicidae), Aedes albopictus (Skuse) and Aedes japonicus (Theobald), across the altitudinal range of Mt. Konpira, Nagasaki, Japan, a location within their native range, where Aedes flavopictus Yamada, formerly a rare species, has now become dominant. Spatial abundance patterns of the three species suggest that temperature is an important factor influencing their adult distribution across the altitudinal range of Mt. Konpira. Temporal abundance patterns, by contrast, were associated with rainfall and showed signals of density-dependent regulation in the three species. The spatial and temporal analysis of abundance patterns showed that Ae. flavopictus and Ae. albopictus were negatively associated, even when accounting for differential impacts of weather and other environmental factors in their co-occurrence patterns. Our results highlight a contingency in the expansion of invasive vectors, the potential emergence of changes in their interactions with species in their native communities, and raise the question of whether these changes might be useful to predict the emergence of future invasive vectors.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Brunsdon C, Comber L (2015) An introduction to R for spatial analysis and mapping. Sage Publications LTD, London

    Google Scholar 

  • Chaves LF (2016) Climate change and the biology of insect vectors of human pathogens. In: Johnson S, Jones H (eds) Invertebrates and global climate change. Wiley, Chichester, In Press

    Google Scholar 

  • Chaves LF, Añez N (2016) Nestedness patterns of sand fly (Diptera: Psychodidae) species in a neotropical semi-arid environment. Acta Trop 153:7–13

    Article  Google Scholar 

  • Chaves LF, Koenraadt CJM (2010) Climate change and highland malaria: fresh air for a hot debate. Q Rev Biol 85:27–55

    Article  Google Scholar 

  • Chaves, L.F., Hamer, G.L., Walker, E.D., Brown, W.M., Ruiz, M.O. & Kitron, U.D. (2011). Climatic variability and landscape heterogeneity impact urban mosquito diversity and vector abundance and infection. Ecosphere, 2, art70.

  • Chaves LF, Morrison AC, Kitron UD, Scott TW (2012) Nonlinear impacts of climatic variability on the density-dependent regulation of an insect vector of disease. Glob Chang Biol 18:457–468

    Article  Google Scholar 

  • Chaves LF, Scott TW, Morrison AC, Takada T (2014) Hot temperatures can force delayed mosquito outbreaks via sequential changes in Aedes aegypti demographic parameters in autocorrelated environments. Acta Trop 129:15–24

    Article  Google Scholar 

  • Chaves LF, Imanishi N, Hoshi T (2015) Population dynamics of Armigeres subalbatus (Diptera: Culicidae) across a temperate altitudinal gradient. Bull Entomol Res 105:589–597

    Article  CAS  Google Scholar 

  • Egizi A, Fefferman NH, Fonseca DM (2015) Evidence that implicit assumptions of ‘no evolution’ of disease vectors in changing environments can be violated on a rapid timescale. Biological Sciences, Philosophical Transactions of the Royal Society of London B, p 370

    Google Scholar 

  • Eisen L, Bolling BG, Blair CD, Beaty BJ, Moore CG (2008) Mosquito species richness, composition, and abundance along habitat-climate-elevation gradients in the Northern Colorado Front Range. J Med Entomol 45:800–811

    Article  Google Scholar 

  • Eshita Y, Kurihara T, Ogata T, Oya A (1982) Studies on the susceptibility of mosquitoes to dengue virus: I. Susceptibility of Japanese mosquitoes to the virus Japanese Journal of Sanitary Zoology 33:61–64

    Google Scholar 

  • Faraway JJ (2006) Extending the linear model with R: generalized linear, mixed effects and nonparametric regression models. CRC Press, Boca Raton

    Google Scholar 

  • Gaunt CMT, Mutebi J-P, Munstermann LE (2004) Biochemical taxonomy and enzyme electrophoretic profiles during development, for three morphologically similar Aedes species (Diptera: Culicidae) of the subgenus Stegomyia. J Med Entomol 41:23–32

    Article  Google Scholar 

  • Gotelli NJ, McCabe DJ (2002) Species co-occurrence: a meta-analysis of J. M Diamond’s assembly rules model Ecology 83:2091–2096

    Google Scholar 

  • Hernandez MJ (2009) Disentangling nature, strength and stability issues in the characterization of population interactions. J Theor Biol 261:107–119

    Article  Google Scholar 

  • Hodkinson ID (2005) Terrestrial insects along elevation gradients: species and community responses to altitude. Biol Rev Camb Philos Soc 80:489–513

    Article  Google Scholar 

  • Hoshi T, Higa Y, Chaves LF (2014a) Uranotaenia novobscura ryukyuana (Diptera: Culicidae) population dynamics are denso-dependent and autonomous from weather fluctuations. Ann Entomol Soc Am 107:136–142

  • Hoshi T, Imanishi N, Higa Y, Chaves LF (2014b) Mosquito biodiversity patterns around urban environments in south-central Okinawa Island, Japan. J Am Mosq Control Assoc 30:260–267

  • Juliano SA (2009) Species interactions among larval mosquitoes: context dependence across habitat gradients. Annu Rev Entomol 54:37–56

    Article  CAS  Google Scholar 

  • Juliano SA, Lounibos LP (2005) Ecology of invasive mosquitoes: effects on resident species and on human health. Ecol Lett 8:558–574

    Article  Google Scholar 

  • Juliano S, Lounibos L, O’Meara G (2004) A field test for competitive effects of Aedes albopictus on A. aegypti in South Florida: differences between sites of coexistence and exclusion? Oecologia 139:583–593

    Article  Google Scholar 

  • Kamimura K (1968) The distribution and habit of medically important mosquitoes of Japan. Japanese J Sanit Zool 19:15–34

    Article  Google Scholar 

  • Kaufman MG, Fonseca DM (2014) Invasion biology of Aedes japonicus japonicus (Diptera: Culicidae). Annu Rev Entomol 59:31–49

    Article  CAS  Google Scholar 

  • Khibnik AI, Kondrashov AS (1997) Three mechanisms of Red Queen dynamics. Proc R Soc B Biol Sci 264:1049–1056

    Article  Google Scholar 

  • Kim HC, Klein TA, Lee WJ, Collier BW, Chong ST, Sames WJ et al (2007) Mosquito species distribution and larval breeding habitats with taxonomic identification of Anopheline mosquitoes in Korea. Entomol Res 37:29–35

    Article  Google Scholar 

  • Kobayashi M, Nihei N, Kurihara T (2002) Analysis of northern distribution of Aedes albopictus (Diptera:Culicidae) in Japan by geographical information system. J Med Entomol 39:4–11

    Article  CAS  Google Scholar 

  • Kuhn M, Johnson K (2013) Applied predictive modeling. Springer, New York

    Book  Google Scholar 

  • Kurashige Y (1961a) Ecological studies on mosquitoes in the bamboo groves of Tochigi Prefecture : III. Mosquito larvae in the stumps of bamboo (Madake) in Utsunomiya City. Japanese J Sanit Zool 12:30–35

  • Kurashige Y (1961b) Ecological studies on mosquitoes in the bamboo groves of Tochigi Prefecture: IV. Mosquito larvae in the bamboo groves in summer Japanese Journal of Sanitary Zoology 12:119–124

  • Larson R, Edwards BH (2013) Calculus., Brooks Cole Pacific Grove

    Google Scholar 

  • Levins R (1968) Evolution in changing environments. Some theoretical explorations. Princeton University Press, Princeton

    Google Scholar 

  • Lounibos LP (2002) Invasions by insect vectors of human disease. Annu Rev Entomol 47:233–266

    Article  CAS  Google Scholar 

  • Lounibos LP, O’Meara GF, Juliano SA, Nishimura N, Escher RL, Reiskind MH et al (2010) Differential survivorship of invasive mosquito species in South Florida Cemeteries: do site-specific microclimates explain patterns of coexistence and exclusion? Ann Entomol Soc Am 103:757–770

    Article  Google Scholar 

  • Makiya K (1974) Population dynamics of mosquitoes in Nagoya district B. Larval and imaginal populations of Aedes albopictus (Skuse) in a cemetery of Nagoya City. Japanese J Sanit Zool 25:41–49

    Article  Google Scholar 

  • Mangel M (2006) The theoretical biologist’s toolbox: quantitative methods for ecology and evolutionary biology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Melbourne BA, Hastings A (2008) Extinction risk depends strongly on factors contributing to stochasticity. Nature 454:100–103

    Article  CAS  Google Scholar 

  • Miyagi I, Toma T (1989) Experimental crossing of Aedes albopictus, Aedes flavopictus downsi and Aedes riversi (Diptera : Culicidae) occurring in Okinawajima, Ryukyu Islands, Japan. Japanese J Sanit Zool 40:87–95

    Article  Google Scholar 

  • Mogi M (1996) Overwintering strategies of mosquitoes (Diptera: Culicidae) on warmer islands may predict impact of global warming on Kyushu, Japan. J Med Entomol 33:438–444

    Article  CAS  Google Scholar 

  • Mogi M, Tuno N (2014) Impact of climate change on the distribution of Aedes albopictus (Diptera: Culicidae) in northern Japan: retrospective analyses. J Med Entomol 51:572–579

    Article  Google Scholar 

  • Mori A, Wada Y (1978) The seasonal abundance of Aedes albopictus in Nagasaki. Tropical Medicine 20:29–37

    Google Scholar 

  • Moriya K (1974) Seasonal trends of field population of mosquitoes with ovitrap in Kanagawa Prefecture : 1) Comparison of the populations of four residential areas in Kamakura City in 1971. Japanese J Sanit Zool 25:237–244

    Article  Google Scholar 

  • Omori N, Osima M, Bekku H, Fujisaki K (1952) On the mosquitoes found in Nagasaki prefecture. Contributions from the Research Institute of Endemics at Nagasaki University 27:281–284

    Google Scholar 

  • Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669

    Article  Google Scholar 

  • Paupy C, Delatte H, Bagny L, Corbel V, Fontenille D (2009) Aedes albopictus, an arbovirus vector: from the darkness to the light. Microbes Infect 11:1177–1185

    Article  CAS  Google Scholar 

  • Post E (2013) Ecology of climate change: the importance of biotic interactions. Princeton University Press, Princeton

    Book  Google Scholar 

  • Proestos Y, Christophides GK, Ergüler K, Tanarhte M, Waldock J, Lelieveld J (2015) Present and future projections of habitat suitability of the Asian tiger mosquito, a vector of viral pathogens, from global climate simulation. Philos Trans R Soc Lond B Biol Sci 370:20130554

    Article  Google Scholar 

  • Shiraishi S (2011) Field collections of mosquito larvae in 2009 and 2010 in Ehime Prefecture, western Japan. Med Entomol Zool 62:109–116

    Article  Google Scholar 

  • Shumway RH, Stoffer DS (2011) Time series analysis and its applications, 3rd edn. Springer, New York

    Book  Google Scholar 

  • Sota T, Mogi M, Hayamizu E (1992) Seasonal distribution and habitat selection by Aedes albopictus and Ae riversi (Diptera, Culicidae) in Northern Kyushu, Japan. J Med Entomol 29:296–304

    Article  CAS  Google Scholar 

  • Stevens GC (1992) The elevational gradient in altitudinal range: an extension of Rapoport’s latitudinal rule to altitude. Am Nat 140:893–911

    Article  CAS  Google Scholar 

  • Sunahara T, Mogi M (2002) Variability of intra‐and interspecific competitions of bamboo stump mosquito larvae over small and large spatial scales. Oikos 97:87–96

    Article  Google Scholar 

  • Taira K, Toma T, Tamashiro M, Miyagi I (2012) DNA barcoding for identification of mosquitoes (Diptera: Culicidae) from the Ryukyu Archipelago, Japan. Med Entomol Zool 63:289–306

    Article  Google Scholar 

  • Tanaka K, Mizusawa K, Saugstad ES (1979) A revision of the adult and larval mosquitoes of Japan (including the Ryukyu Archipelago and the Ogasawara Islands) and Korea (Diptera: Culicidae). Contributions of the American Entomological Institute 16:1–987

    Google Scholar 

  • Toma T, Miyagi I, Crabtree MB, Miller BR (2002) Investigation of the Aedes (Stegomyia) flavopictus Complex (Diptera: Culicidae) in Japan by Sequence Analysis of the Internal Transcribed Spacers of Ribosomal DNA. J Med Entomol 39:461–468

    Article  CAS  Google Scholar 

  • Tsuda Y, Takagi M, Wada Y (1994) Ecological study on mosquito communities in tree holes in Nagasaki, Japan, with special reference to Aedes albopictus (Diptera: Culicidae). Japanese J Sanit Zool 45:103–111

    Article  Google Scholar 

  • Tsuda Y, Maekawa Y, Saita S, Hasegawa M, Takagi M (2003) Dry ice-trap collection of mosquitoes flying near a tree canopy in Nagasaki, Japan, with special reference to Aedes albopictus (Skuse) and Culex pipiens pallens Coquillett (Diptera : Culicidae). Med Entomol Zool 54:325–330

    Article  Google Scholar 

  • Turchin P (2003) Complex population dynamics. Princeton University Press, Princeton

    Google Scholar 

  • Vamosi SM, Heard SB, Vamosi JC, Webb CO (2009) Emerging patterns in the comparative analysis of phylogenetic community structure. Mol Ecol 18:572–592

    Article  CAS  Google Scholar 

  • Venables WN, Ripley BD (2002) Modern applied statistics with S. Springer, New York

    Book  Google Scholar 

  • Yamada S (1921) Descriptions of ten new species of Aedes found in Japan, with notes on the relation between some of these mosquitoes and the larva of Filaria bancrofti Cobbold. Annotationes Zoologicae Japonenses 10:45–81

    Google Scholar 

  • Yamauchi T (2010) Mosquito species (Diptera: Culicidae) collected from the inhabited islands and trunk of Uwajima City, Shikoku, Japan. Med Entomol Zool 61:121–124

    Article  Google Scholar 

  • Yamauchi T (2013) Mosquitoes found along the coast of Toyama Prefecture, Japan. Pestology 28:17–20

    Google Scholar 

  • Yang G-J, Bradshaw C, Whelan P, Brook B (2008) Importance of endogenous feedback controlling the long-term abundance of tropical mosquito species. Popul Ecol 50:293–305

    Article  Google Scholar 

  • Zea Iriarte WL, Tsuda Y, Wada Y, Takagi M (1991) Distribution of mosquitoes on a hill of Nagasaki city, with emphasis to the distance from human dwellings. Tropical Medicine 33:55–60

    Google Scholar 

Download references

Acknowledgments

This study was funded by Sumitomo Foundation grant No. 153107 to LFC. Nagasaki City direction of green areas kindly provided all relevant permits to perform the study. Tomonori Hoshi and Nozomi Imanishi performed the net sweeping sampling and helped with mosquito identification. Finally, Ms. Junko Sakemoto provided valuable administrative support.

Author information

Authors and Affiliations

  1. Nagasaki University Institute of Tropical Medicine (NEKKEN), Sakamoto 1-12-4, Nagasaki, Japan

    Luis Fernando Chaves

  2. Programa de Investigación en Enfermedades Tropicales (PIET), Escuela de Medicina Veterinaria, Universidad Nacional, Apartado Postal 304-3000, Heredia, Costa Rica

    Luis Fernando Chaves

Authors
  1. Luis Fernando Chaves
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Luis Fernando Chaves.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplement S1

(DOCX 29 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chaves, L.F. Globally invasive, withdrawing at home: Aedes albopictus and Aedes japonicus facing the rise of Aedes flavopictus . Int J Biometeorol 60, 1727–1738 (2016). https://doi.org/10.1007/s00484-016-1162-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00484-016-1162-7

Keywords

Search

Navigation