Cited by 1,027Mosquito-borne diseases and controlSpecies Distribution and Climate ChangeVector-borne infectious diseases

Spread of The Tiger: Global Risk of Invasion by The Mosquito Aedes albopictus

Open access
Benedict, Mark Q., Levine, Rebecca S., Hawley, William A., Lounibos, L. Philip·2007·Vector-Borne and Zoonotic Diseases

Abstract

Aedes albopictus, commonly known as the Asian tiger mosquito, is currently the most invasive mosquito in the world. It is of medical importance due to its aggressive daytime human-biting behavior and ability to vector many viruses, including dengue, LaCrosse, and West Nile. Invasions into new areas of its potential range are often initiated through the transportation of eggs via the international trade in used tires. We use a genetic algorithm, Genetic Algorithm for Rule Set Production (GARP), to determine the ecological niche of Ae. albopictus and predict a global ecological risk map for the continued spread of the species. We combine this analysis with risk due to importation of tires from infested countries and their proximity to countries that have already been invaded to develop a list of countries most at risk for future introductions and establishments. Methods used here have potential for predicting risks of future invasions of vectors or pathogens.

AI snapshot

Written from the paper’s full text.

TL;DR

The paper uses GARP ecological niche modeling to predict the global potential range of *Aedes albopictus* and combines that with used-tire import and border-proximity data to rank countries at risk of future introduction and establishment. It identifies Mainland Australia, New Zealand, and South Africa as the uninfested countries most at risk among those with suitable data.

Key findings

  • The native Asian range model used 202 occurrence points; 200 of 202 fell within the predicted range versus 147 expected by chance (χ² = 19.1, 1 df, p < 0.0001), and 175 points (87%) fell in pixels where 6 or more of 10 GARP models predicted presence.
  • Projected occurrence points fell within majority-model pixels for Central America (92%) and Africa (86%), but only 17% for Europe, where 10% fell in pixels with no model agreement; U.S. predictions missed only 2 or 14 of 1011 counties, and Brazil had 4334 of 5501 points in majority-model pixels.
  • Among 31 uninfested countries with suitable data, Mainland Australia, New Zealand, and South Africa were clearly most at risk; the Netherlands and Canada had high tire imports and borders with infested countries but were sufficiently cold that disease risk was low.
  • At 408 random geo-referenced occurrence points worldwide, annual mean temperature ranged from 5.0–28.5°C, mean annual precipitation from 29.2–445.3 cm, and ground-frost days per month from 0–138.

Methods

  • Occurrence data included 206 Asian points (164 literature records plus 42 original collections; 4 unusable), plus exotic records of 181 unique points worldwide, 5574 in Brazil, and 1033 U.S. counties; 11 environmental layers at 0.1-degree resolution were used.
  • GARP produced 10 models per prediction map, summed to assign pixels values of 0–10; models used up to 100,000 iterations and a convergence criterion of 0.0001, and the native-range niche was projected onto five geographic zones.
  • Risk assessment selected ecologically suitable countries, then considered extent of favorable area, used-tire shipments from infested countries for 2002–2004 (UN COM-TRADE, HS02-401220), and shared borders with infested countries; cluster analysis examined precipitation and temperature by multiple regression above and below 30 degrees north latitude.

Limitations

  • The paper states that lumping diapausing and non-diapausing types means models predict potential distribution in toto rather than for one type, and that annual climate values may under- or overpredict habitat whose seasonal suitability is not reflected in annual averages.
  • The paper also states that coarse resolution and lack of sampling or reporting may cause overprediction, that tire import data were unavailable for some countries, and that its risk method is one of many reasonable approaches.
  • Evident from the text: occurrence data are presence-only and do not consider abundance, and some small islands below the resolution of the model climate layers were excluded from analysis.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1089/vbz.2006.0562

Cites

54 of 54 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 12 cited sources checked · 0 supported · 0 flagged

  • Findingown data
    § RESULTS AND DISCUSSION

    The distribution of observed occurrences was not random relative to the predicted distribution (χ2 19.1, 1 df, p < 0.0001).

    “In fact, 200 of 202 fell within the predicted range (χ2 19.1, 1 df, p < 0.0001) confirming that the GARP predictions were not random.”
    Quote in the paperSubstantial claim
  • Findingown data
    § RESULTS AND DISCUSSION

    For the United States, two GARP prediction maps predicted presence in all but two or 14 of 1011 counties in which Ae. albopictus has been reported.

    “Two GARP prediction maps (as described above), respectively predicted presence in all but two or 14 of 1011 counties in the United States in which Ae. albopictus has been reported (Fig. 3).”
    Quote in the paperSubstantial claim
  • Findingown data
    § MATERIALS AND METHODS

    All countries in which Ae. albopictus establishment has occurred have some areas in which there was at least weak prediction map agreement.

    “We observed that all countries in which establishment has occurred have some areas in which there was at least weak prediction map agreement, therefore we excluded countries not having any models agreeing on establishment from further consideration.”
    Quote in the paperSubstantial claim
  • Findingown data
    § RESULTS AND DISCUSSION

    Temperature and humidity values at Ae. albopictus occurrence points demonstrate an ability to inhabit either relatively cold and dry or warm and wet climates.

    “Temperature and humidity values at Ae. albopictus occurrence points demonstrate an ability to inhabit either relatively cold and dry or warm and wet climates (Fig. 5, Table 2), therefore risk of establishment depends to some extent on the origin of the mosquitoes.”
    Quote in the paperSubstantial claim
  • Findingown data
    § RESULTS AND DISCUSSION

    In Brazil, 4334 of 5501 occurrence points fell within pixels in which a majority of models agreed on presence.

    “Of all points, 4334 of 5501 fell within pixels in which a majority of models agreed on presence.”
    Quote in the paperNot a substantial claim
  • May combine two claims. 17
  • Classified as probably not a substantial claim. 1
  • May combine two claims.

    Findingown data
    § RESULTS AND DISCUSSION

    Ae. albopictus can establish in areas with annual mean temperatures of 5°C-28.5°C and annual rainfall as low as 29 cm.

    “Environmental data for Ae. albopictus occurrence demonstrate that it can establish in areas with much lower annual mean temperatures (5°C–28.5°C ) and less rainfall (as low as 29 cm annually) than has been suspected.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data
    § RESULTS AND DISCUSSION

    Democratic Republic of Congo, Mozambique, Angola, the Central African Republic, Ethiopia, Congo, Côte d' Voire, and Gabon contain extensive areas of suitable niche but had no tire data available.

    “Additional countries for which no tire data were available also contain extensive areas of suitable niche: Democratic Republic of Congo, Mozambique, Angola, the Central African Republic, Ethiopia, Congo, Côte d’ Voire, and Gabon.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data
    § RESULTS AND DISCUSSION

    In Central America and Africa, 92% and 86% of occurrence points respectively fell within pixels predicted by a majority of models, and most were within pixels predicted by 9 or 10 models.

    “The results for Central America and Africa were similar: 92% and 86% of the points, respectively, fell within pixels predicted by a majority of the models, and by far most were within pixels predicted by 9 or 10 models.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingreasoning
    § RESULTS AND DISCUSSION

    In Europe, only 17% of occurrence points fell within pixels predicted by a majority of models, and 10% fell within pixels for which no models predicted presence, many in northern Italy.

    “In contrast, because few pixels in Europe were predicted for presence by a majority of models, only 17 % fell in this range, and 10% fell within pixels for which no models predicted presence, many of these in northern Italy.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingcitation
    § RESULTS AND DISCUSSION

    Mitchell (1995) suggested that the maximum distribution of Ae. albopictus included limited parts of Spain, Portugal, France, Italy, Greece, Albania, Macedonia, Bulgaria, and Turkey; however, this model did not predict occupied habitat in both northern Italy and France predicted by GARP.

    “Mitchell (1995) suggested that the maximum distribution of Ae. albopictus included limited parts of Spain, Portugal, France, Italy, Greece, Albania, Macedonia, Bulgaria, and Turkey. However, this model did not predict occupied habitat in both northern Italy and France predicted by GARP.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Mitchell 1995

      Not checked in the free run.

  • May combine two claims.

    Findingown data
    § RESULTS AND DISCUSSION

    The −5°C January isotherm considered by Nawrocki and Hawley (1987) as a liberal estimate of the northern distribution limit is similar to that predicted using GARP, though GARP resulted in more detail and added a prediction of the western limit of potential habitat in the Midwest.

    “The −5°C January isotherm, which Nawrocki and Hawley (1987) considered a liberal estimate of the northern distribution limit, is similar to that which we predict using GARP, though the latter method resulted in more detail and added a prediction of the western limit of potential habitat in the Midwest.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Nawrocki and Hawley 1987

      Not checked in the free run.

  • May combine two claims.

    Findingreasoning
    § RESULTS AND DISCUSSION

    Belize, Costa Rica, and Haiti have not reported Ae. albopictus yet all are surrounded by, or adjacent to, infested countries and provide suitable niche.

    “In the Caribbean and Central America, Belize, Costa Rica, and Haiti have not reported Aedes albopictus yet all are surrounded by, or adjacent to, infested countries and they themselves provide suitable niche.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationreasoning
    § RESULTS AND DISCUSSION

    The Netherlands and Canada have high tire imports and border infested countries but are sufficiently cold that disease risk is low.

    “Two other high tire import countries—The Netherlands and Canada—have an additional risk factor of bordering on infested countries but are sufficiently cold that disease risk is low.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Interpretationreasoning
    § MATERIALS AND METHODS

    Peru, Uruguay, Venezuela, Guyana, and French Guiana are likely to be imminently infested due to proximity of geo-referenced collections near or on the country border.

    “We included as infested all countries that have been reported (Table 1) and five more that—although unreported—are likely to be imminently infested due to the proximity of geo-referenced collections near or on the country border: Peru, Uruguay, Venezuela, Guyana, and French Guiana.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Premisecitation
    § INTRODUCTION

    Ae. albopictus is especially prone to inadvertent transport of its relatively cold-hardy and long-lived eggs, and to live in close affiliation with humans and their dwellings and refuse.

    “As an inhabitant of artificial and natural containers, Ae. albopictus is especially prone to inadvertent transport of its relatively cold-hardy and long-lived eggs, and to live in close affiliation with humans and their dwellings and refuse (see reviews by Hawley [1988] and Estrada-Franco [1995]).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Hawley 1988

      Not checked in the free run.

    • cites Estrada-Franco 1995

      Not checked in the free run.

  • May combine two claims.

    Premisecitation
    § Abstract

    Ae. albopictus is a competent vector of dengue, LaCrosse, West Nile, and other viruses, and is of medical importance.

    “It is of medical importance due to its aggressive daytime human-biting behavior and ability to vector many viruses, including dengue, LaCrosse, and West Nile.”
    • Also stated in: § INTRODUCTION · plain
      “It ranks second only to Ae. aegypti in importance as a vector of dengue virus”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites Mitchell 1995

      Not checked in the free run.

    • cites Shroyer 1986

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning
    § RESULTS AND DISCUSSION

    Chile may escape invasion because its suitable area is isolated from dispersion from neighboring countries and it has banned the importation of used tires.

    “Only Chile differs and may yet escape invasion because the suitable area is isolated from dispersion from neighboring countries. Furthermore, Chile, like some other countries, has banned the importation of used tires, a measure that will provide some protection.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing).

    Interpretationreasoning
    § RESULTS AND DISCUSSION

    Methods used in this analysis have potential for predicting risk from future invasions of vectors or pathogens.

    “Methods used in this analysis have potential for predicting risk from future invasions of vectors or pathogens.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationnone given
    § RESULTS AND DISCUSSION

    The most suitable large areas in Europe occur in France and may be already infested.

    “The most suitable large areas in Europe occur in France and may be already infested.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation
    § RESULTS AND DISCUSSION

    Superior tolerance of Ae. aegypti eggs to humidity and temperature extremes allows this inferior larval competitor to coexist with Ae. albopictus or occupy habitats environmentally unfavorable to the Asian tiger mosquito.

    “Superior tolerance of Ae. aegypti eggs to humidity and temperature extremes allows this inferior larval competitor to coexist with Ae. albopictus or occupy habitats environmentally unfavorable to the Asian tiger mosquito (Braks et al. 2003).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites Braks et al. 2003

      Not checked in the free run.

  • May combine two claims.

    Interpretationreasoning
    § RESULTS AND DISCUSSION

    If the presumption of imminent or actual infestation of five countries bordering Brazil is correct, only Suriname, Ecuador, and Chile remain uninfested, and all have large areas of suitable niche.

    “If our presumption of the imminent or actual infestation of five countries bordering Brazil is correct, only three remain uninfested, and all have large areas of suitable niche: Suriname, Ecuador, and Chile.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Interpretationreasoning
    § RESULTS AND DISCUSSION

    The Bahamas and Jamaica may escape establishment because both are isolated, but no tire importation data were available.

    “However, the Bahamas and Jamaica may yet escape establishment because both are isolated, but no tire importation data were available.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation
    § RESULTS AND DISCUSSION

    The egg stage of Ae. albopictus suffers high mortality in conditions of low humidity and high temperature, and the interaction between these mortality factors may account in part for the distribution of U.S. populations in relation to rainfall and temperature and the large gap in the midcontinental range.

    “The egg stage of Ae. albopictus suffers high mortality in conditions of low humidity and high temperature, and the known interaction between these mortality factors (Juliano et al. 2002) may account in part for the distribution of U.S. populations of the species in relation to rainfall and temperature (Fig. 1) and the large gap in the midcontinental range (Fig. 3).”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites Juliano et al. 2002

      Not checked in the free run.

18 of 18
  • The paper relies on this without support.

    Shared borders with infested countries increase the risk of introduction of Ae. albopictus.

    “Among the remaining ecologically suitable countries, three risk factors were considered: (1) the extent of favorable area for establishment, (2) probable means of introduction via used tire shipments, and (3) shared borders with infested countries.”
  • The paper relies on this without support.

    Globalization of cargo trade and increasing air travel means that opportunities for introductions of exotic organisms including pathogens and their hosts are abundant.

    “Globalization of cargo trade and increasing air travel means that opportunities for introductions of exotic organisms including pathogens and their hosts are abundant.”
2 of 2

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Increasing temperatures in Europe have allowed the widespread establishment of exotic, daybiting mosquito species such as Ae. albopictus.

    “Finally, increasing temperatures in Europe also allowed the widespread establishment of exotic, daybiting mosquito species such as Ae. albopictus [79–81], which is an important potential vector for D. immitis and D. repens and the establishment of the species in numerous European regions has been linked to increased Dirofilaria circulation [22].”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • South Africa appears in an establishments table despite a contrary footnote

    Minor

    South Africa is marked with footnote b in Table 1, whose heading says the listed countries had established populations. The footnote says its introduction did not result in establishment.

  • U.S. county totals differ

    Minor

    The data section reports records from 1,033 U.S. counties, whereas the results give 1,011 as the number of counties in which the mosquito was reported. No exclusion explaining the 22-county difference is stated.

2 of 2

Cites

Flagged first, then by citations

Research works printed but not linked: 23

  1. Adhami J, 1998, J Am Mosq Control Assoc, 14, 340
  2. Anonymous, 1989, Mexico. MMWR, 38, 445
  3. Broche RG, 1999, J Am Mosq Control Assoc, 15, 569
  4. Cornel A, 1991, J Am Mosq Control Assoc, 7, 107
  5. Estrada-Franco J., 1995, PAHO Technical Paper, 42
  6. Hawley WA, 1988, J Am Mosq Control Assoc, 4, 1
  7. Knudsen A, 1996, J Am Mosq Control Assoc, 12, 177
  8. Le Maitre A, 1983, West Indies. J Am Mosq Control Assoc, 43, 21
  9. Madon MB, 2002, J Vector Ecol, 27, 149
  10. Mitchell C, 1995, J Vector Ecol, 20, 44
  11. Nawrocki SJ, 1987, J Am Mosq Control Assoc, 3, 314
  12. Ogata K, 1996, J Am Mosq Control Assoc, 12, 503
  13. Peña CJ, 1993, Vector Ecol Newsl, 24
  14. Reiter P, 1998, J Am Mosq Control Assoc, 14, 83
  15. Reiter P, 1987, J Am Mosq Control Assoc, 3, 494
  16. Rossi GC, 1999, J Am Mosq Control Assoc, 15, 422
  17. Sabatini A, 1990, Parassitologia, 32, 301
  18. Savage HM, 1992, J Am Mosq Control Assoc, 8, 101
  19. Schaffner F, 2004, J Am Mosq Control Assoc, 20, 201
  20. Shroyer DA, 1986, J Am Mosq Control Assoc, 2, 424
  21. Sota T, 1992, Entomolexpappl, 63, 155
  22. Sprenger D, 1986, Texas. J Am Mosq Control Assoc, 2, 217
  23. Velez Iñ, 1998, Colombia. Biomedica, 18, 182

Cited by

Sorted by citations

Authors
Benedict, M. Q., Levine, R. S., Hawley, W. A., & Lounibos, L. P.
Affiliations
  • Centers for Disease Control and Prevention (US)
  • University of Florida (US)
Venue
Vector-Borne and Zoonotic Diseases
Published
2007-03
Volume
7
Issue
1
Pages
76-85
ISSN
  • 1530-3667 (ISSN-L)
  • 1557-7759
OpenAlex
W2023473182
Cited by
1,027
References
54
Citations by year
2026: 37 · 2025: 32 · 2024: 54 · 2023: 60 · 2022: 48 · 2021: 57 · 2020: 73 · 2019: 68 · 2018: 55 · 2017: 73 · 2016: 70 · 2015: 74 · 2014: 71 · 2013: 75 · 2012: 52
FWCI
30.89
Type
journal article
Language
en
Open access
Locations
  • Vector-Borne and Zoonotic Diseases (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
National Institute of Allergy and Infectious Diseases (R01-AI44793, R01AI044793)
Topics
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Mosquito-borne diseases and control
  • Physical Sciences › Environmental Science › Ecological Modeling › Species Distribution and Climate Change
  • Life Sciences › Immunology and Microbiology › Parasitology › Vector-borne infectious diseases
Keywords
Aedes albopictus, invasive species, ecological niche modeling, dengue vector, West Nile virus, La Crosse virus, vector-borne disease vectors
MeSH terms
Aedes, Algorithms, Animals, Commerce, Computer Simulation, Disease Reservoirs, Ecology, Forecasting, Humans, Insect Bites and Stings, Insect Vectors, Mosquito Control, Population Growth, Predictive Value of Tests, Risk Factors, Global Health

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